INVASION RISK OF THE LIONFISHES PTEROIS...
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INVASION RISK OF THE LIONFISHES PTEROIS, DENDROCHIRUS, AND PARAPTEROIS By TIMOTHY J. LYONS A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2018
Transcript of INVASION RISK OF THE LIONFISHES PTEROIS...
INVASION RISK OF THE LIONFISHES PTEROIS, DENDROCHIRUS, AND PARAPTEROIS
By
TIMOTHY J. LYONS
A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE
UNIVERSITY OF FLORIDA
2018
© 2018 Timothy J. Lyons
To my mentors, friends, and family
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ACKNOWLEDGMENTS
I thank the members of my supervisory committee. Dr. Jeff Hill has continually
guided my research by providing me with the tools to shape my own success, and has
taught me that independence, self-motivation, and critical thinking are key virtues. Dr.
Quenton Tuckett has spent many long hours discussing, editing, and guiding my
scientific thought and writing, for which I am extremely grateful. Dr. Daryl Parkyn
continues to serve as a mentor and has contributed to my development as a scientist.
I also thank those who have assisted in my research project. I thank Liz Groover,
Michael Sipos, Taylor Lipscomb, and Shane Ramee for their continual support inside
and outside of the lab. I thank Craig Watson, Dr. Matthew Dimaggio, Dr. Roy Yanong,
Dr. Kathleen Hartman, Micah Alo, Amy Wood, Cynjun Diehl, and all other faculty and
staff at the University of Florida’s Tropical Aquaculture Laboratory for all their hard work
and for the invaluable lessons I will take with me.
Finally, I thank the friends and family that have provided me with support
throughout my career, especially my girlfriend Nina Doyle and her family for their
unwaning support and enthusiasm, and my closest friends Hayden Bonnen, Matthew
Barr, Michael Rodriguez, Perry Knight, Robert Zinzell, and Reinaldo Sanchez. I thank
my parents for the sacrifices they have made for me to be where I am.
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TABLE OF CONTENTS page
ACKNOWLEDGMENTS .................................................................................................. 4
LIST OF TABLES ............................................................................................................ 7
LIST OF FIGURES .......................................................................................................... 8
LIST OF ABBREVIATIONS ............................................................................................. 9
ABSTRACT ................................................................................................................... 10
CHAPTER
1 INTRODUCTION .................................................................................................... 12
2 DATA QUALITY AND QUANTITY FOR INVASIVE SPECIES: A CASE STUDY OF THE LIONFISHES ............................................................................................ 17 Methods .................................................................................................................. 20
Standardized Literature Review ....................................................................... 20 Bioprofiles ......................................................................................................... 21 Characterizing Literature .................................................................................. 22
Results .................................................................................................................... 23 Standardized Literature Review ....................................................................... 23
Bioprofiles ......................................................................................................... 25 Discussion .............................................................................................................. 26
3 CHARACTERIZING THE US TRADE IN LIONFISHES .......................................... 40 Methods .................................................................................................................. 44
Data Collection ................................................................................................. 45 Retail Surveys .................................................................................................. 46
Results .................................................................................................................... 47 Discussion .............................................................................................................. 49
4 RISK SCREEN OF LIONFISHES PTEROIS, DENDROCHIRUS, AND PARAPTEROIS FOR COASTAL WATERS OF THE GULF AND ATLANTIC ........ 62
Methods .................................................................................................................. 64 Results .................................................................................................................... 67 Discussion .............................................................................................................. 71
5 CONCLUSION ........................................................................................................ 79
APPENDIX: AQUATIC SPECIES INVASIVENESS SCREENING KIT QUESTION SCHEME ................................................................................................................ 84
LIST OF REFERENCES ............................................................................................... 87
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BIOGRAPHICAL SKETCH .......................................................................................... 101
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LIST OF TABLES
Table page 2-1 Criteria for 11 content categories characteristic of the body of literature on
the subfamily Pteroinae ...................................................................................... 34
2-2 Frequency of data points and respective category codes returned from a standardized literature search for 18 species of lionfish using the Web of Science Database .............................................................................................. 35
2-3 Frequency of data points and respective category codes returned during a standardized search for the invasive complex P. volitans/P. miles prior to establishment, during the early invasion, and post-establishment, conducted using the Web of Science Database ................................................................... 36
2-4 Types of literature used in the formation of bioprofiles for 14 species of lionfish as part of a risk assessment for Florida .................................................. 37
3-1 Maximum body size of Pterois, Dendrochirus, and Parapterois present in the U.S. ornamental aquarium trade ......................................................................... 55
4-1 Aquatic Species Invasiveness Screening Kit results applied to the State of Florida for 14 species of lionfishes in the genera Pterois, Dendrochirus, and Parapterois. ........................................................................................................ 76
A-1 Aquatic Species Invasiveness Screening Kit question scheme .......................... 84
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LIST OF FIGURES
Figure page 2-1 Number of articles and data points for 18 species of lionfish returned by Web
of Science ........................................................................................................... 38
2-2 Frequency of articles published each year from 1900-2017 for the invasive lionfish complex P. volitans/P. miles and for 16 other species of lionfish ........... 39
3-1 Eight species of lionfishes present in the U.S. ornamental fish trade from April 2016-2017 .................................................................................................. 56
3-2 Total volume of each species of lionfish imported and recorded in the U.S. Fish and Wildlife Service’s LEMIS database from April 2016-2017 .................... 57
3-3 Species composition and relative volume of lionfish trade for six major receiving ports .................................................................................................... 58
3-4 Monthly variability for the top five species of lionfishes by import volume from April 2, 2016 to April 1, 2017. ............................................................................. 59
3-5 Total volume of lionfish received at ports in the United States between April 2, 2016-April 1, 2017 .......................................................................................... 60
3-6 Percent occurrence of six species of lionfish identified in U.S. retail aquarium stores in 10 coastal states during a two-week survey ......................................... 61
4-1 Mean (±SD) basic risk assessment and climate change assessment AS-ISK scores for 14 species of ornamental lionfishes ................................................... 77
4-2 Mean (±SD) score partitioning for nine Aquatic Species Invasiveness Screening Kit (AS-ISK) scoring categories ......................................................... 78
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LIST OF ABBREVIATIONS
ANSTF Aquatic Nuisance Species Task Force
AS-ISK Aquatic Species Invasiveness Screening Kit
BRA Basic Risk Assessment
CCA Climate Change Assessment
CF Confidence Factor
CFR Code of Federal Regulations
DAR Division of Aquatic Resources
EPA Environmental Protection Agency
FISK Fish Invasiveness Screening Kit
FOIA Freedom of Information Act
FWC Florida Fish and Wildlife Conservation Commission
FWRI Fish and Wildlife Research Institute
GBIF Global Biodiversity Information Facility
LEMIS Law Enforcement Management Information System
RA Risk Assessment
SD Standard Deviation
SE Standard Error
USGS NAS United States Geological Survey Nonindigenous Aqautic Species Database
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Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science
INVASION RISK OF THE LIONFISHES PTEROIS, DENDROCHIRUS, AND
PARAPTEROIS
By
Timothy J. Lyons
August 2018
Chair: Jeffrey E. Hill Cochair: Quenton M. Tuckett Major: Fisheries and Aquatic Sciences
The trade in marine ornamental fishes includes over 1,800 species, and is a
vector for nonnative species introductions. Given such a large pool of potential invaders,
a targeted approach which evaluates risk for groups of fishes with demonstrated
invasion history can streamline proactive management. Though the establishment of
introduced marine ornamental species is uncommon, the invasion of Pterois volitans
and P. miles in the western Atlantic Ocean clearly demonstrates risk associated with the
marine ornamental industry. These species along with several other lionfishes are
regularly imported into the United States. Therefore, evaluation of the risks associated
with lionfish trade is both timely and practical. The goal of this project was to evaluate
the risk of ornamental lionfishes to inform management by characterizing the literature
on ornamental lionfishes to provide information necessary for risk screening, evaluating
trade patterns to identify the volume and diversity of lionfishes in trade, and assessing
the invasion risk of 14 species of ornamental lionfishes by applying the Aquatic Species
Invasiveness Screening Kit (AS-ISK). The lionfish invasion is widely regarded as one of
the worst marine invasions to date. Despite this, lionfishes that do not exhibit invasion
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history are data poor, trade volume and diversity are lower than previously thought, and
risk associated with the trade of other lionfishes is low with notable exceptions. I identify
P. russelii, P. lunulata, and Dendrochirus brachypterus as species with elevated
invasion risk, and suggest further evaluation of D. brachypterus in a comprehensive risk
assessment for Florida.
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CHAPTER 1 INTRODUCTION
The environmental and ecological damages caused by invasive species, and
costs associated with population control sum to an estimated US$120 billion in the
United States on an annual basis (Pimentel et al. 2005). Inaction or delayed response to
species establishment allows populations to grow and spread beyond a manageable
size, resulting in widespread and often irreversible damage (Lodge et al. 2006). As
such, proactive management frameworks where potentially invasive species are
addressed priori to introduction are receiving greater attention as a cost-effective way to
manage non-native species. Preventing the introduction of non-native species, in
comparison to dedicating large amounts of resources to control programs, remains an
optimal management strategy (Leung et al. 2002).
The aquarium trade is a demonstrated pathway for non-native marine fish
introductions (Semmens et al. 2004). Approximately 20-24 million marine ornamental
fishes are collected annually, including over 1,800 species across 125 families (Wabnitz
et al. 2003; Rhyne et al. 2012). Given the large pool of potential marine invaders and
limited resources, it is a large task to assess the invasion risk of the diverse taxa in
trade, which can make it difficult to identify potentially risky fish or groups of fishes. One
reasonable solution is to take a targeted approach by focusing on those fish or groups
of fishes that are closely related to a species with demonstrated invasion history, which
is a strong predictor of invasion success (Hayes and Barry 2008). A good example of
such a group is the subfamily Pteroinae, which comprises 28 species of lionfishes
across 5 genera and includes the highly invasive Red Lionfish Pterois volitans and Devil
Firefish Pterois miles. Propagule pressure is comprised of the size (i.e. the number of
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individuals per introduction event), the frequency (i.e. the temporal distribution of
discreet introduction events), and the spatial distribution of introduction events
(Simberloff 2009). Such factors must overcome demographic and environmental
stochasticity to result in successful establishment (Shaffer 1987; Lande 1988).
Propagule size is typically low, given the most likely point of release in the pathway is at
the hobbyist level. However, propagule pressure is a strong predictor of establishment
potential, and one variable that has not been fully integrated into current risk screening
tools (Gertzen et al. 2008; Hayes and Barry 2008). Such a lack of propagule
quantification results partly because of difficulties associated with making direct
measures of propagule pressure (Pysek et al. 2010). However, trade volume can be a
useful surrogate measure, providing assessors with an estimate of the number of fishes
available to consumers (Gertzen et al. 2008).
Despite the repeated sightings of over 40 non-native fishes in the environment,
few have successfully established populations outside their native ranges. In Hawaii,
the Peacock Grouper Cephalopholis argus, Blueline Snapper Lutjanus kasmira, and
Blacktail Snapper Lutjanus fulvus have established resulting from early stocking efforts
in the mid 1950’s intended to enhance coastal fisheries productivity (Johnston and
Purkis 2016; Giddens et al. 2017). In the Gulf of Mexico, the Regal Damselfish
Neopomacentrus cyanomos has reached high densities on shallow reef habitat off the
coast of Mexico (González-Gándara and De La Cruz-Francisco 2014; Johnston and
Akins 2016). Others, such as the Blackchin Tilapia Sarotherodon melanotheron can use
and reproduce in brackish coastal waters in Florida with salinities up to 30 parts per
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thousand (Faunce 2000). However, these established species typically have few
documented impacts on ecosystem function or structure in their invaded ranges.
In contrast, the invasive P. volitans and P. miles have documented impacts on
species richness, diversity, and recruitment, in addition to ecosystem structure (Albins
and Hixon 2008; Lesser and Slattery 2011; Albins 2013, 2015). The first reported
incidence of lionfish in the Atlantic occurred in waters off Dania Beach, Florida in 1985,
and they are now distributed throughout the eastern U.S. seaboard to Cape Hatteras,
North Carolina, throughout the Greater Caribbean, Gulf of Mexico, and as far south as
Brazil (Schofield 2010; Ferreira et al. 2015). Additionally, P. miles has established in the
Mediterranean Sea by migrating through the Suez Canal, and continues to spread into
new areas (Kletou et al. 2016; Azzurro et al. 2017). Their rapid population growth and
spread are partly the result of characteristics that are common among other members of
the subfamily Pteroinae. Venomous dorsal, pelvic, and anal spines provide a novel
defense to predation by native fishes (Morris 2009). Additionally, a high fecundity, short
spawning interval, and moderate larval duration enable rapid dispersal (Ahrenholz and
Morris 2010; Morris et al. 2011). Therefore, screening other species in the subfamily
Pteroinae, combined with an evaluation of trade volume provides an accurate first
assessment of risk that can inform future work, and if warranted provide a basis for
regulatory action.
A proactive framework often employs risk screening tools that address the
biology and ecology of the species, the biogeographical and climatic characteristics of
the native range and risk assessment area, and the ecological characteristics of the risk
assessment area (Pheloung et al. 1999). Risk screening tools vary in some aspects, but
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contain several common components, including data standardization (e.g. a guided
question format), replicability, versatility (i.e. applicability to diverse taxa), and
transparency (e.g. response justification and supporting documentation) (Pheloung et
al. 1999; Kolar and Lodge 2002; Lodge et al. 2006). Previous implementation of various
risk screening tools has demonstrated their effectiveness in identifying risky species,
their ability to inform more comprehensive risk assessment, and ultimately their utility in
shaping policy and regulatory action (Kolar and Lodge 2002; Copp et al. 2005; Vander
Zanden et al. 2010; Lawson et al. 2013). For example, the Australian Weed Risk
Assessment has been successfully used to predict risk associated with terrestrial plants
in Australia, New Zealand, Japan, the Czech Republic, and the U.S. (Pheloung et al.
1999; Kato et al. 2006; Křivánek and Pyšek 2006; Gordon et al. 2008).
The most recent addition to the risk screening toolkit is the Aquatic Species
Invasiveness Screening Kit, or AS-ISK (Copp et al. 2016). AS-ISK was adapted from
the widely used and calibrated Fish Invasiveness Screening Kit (Lawson et al. 2013),
and designed as a broad-spectrum tool with applicability to all aquatic taxa. It is
comprised of 49 questions relating to the biological and ecological characteristics of the
species, and the climatic and ecological features of the risk assessment area.
Additionally, 6 questions address potential modifications in invasion risk resulting from
climate change. The tool provides guidance for each question to improve clarity and
reduce subjectivity associated with varied assessor interpretation. In addition,
responses must be justified using existing literature or expert opinion where data are
lacking, further enabling transparency and replicability.
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In chapter one, I address uncertainty in risk evaluation by characterizing the body
of literature pertaining to the lionfishes, identify major data gaps that contribute to
uncertainty, and compare it to literature addressing the invasive complex P. volitans and
P. miles. In chapter two, I evaluate the U.S. trade of lionfishes using three independent
databases and retail surveys in ten coastal states to identify species with potentially
high propagule pressure. In chapter three, I conduct a rapid risk screen of 14 species in
the genera Pterois, Dendrochirus, and Parapterois using the Aquatic Species
Invasiveness Screening Kit to identify potentially risky species for the state of Florida.
Understanding data limitations and integrating trade data at the import and retail level
with current rapid risk screening protocols provides a robust first screening process that
can be applied to a proactive management framework to better inform future
assessment, and prevent the introduction of damaging invasive species.
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CHAPTER 2 DATA QUALITY AND QUANTITY FOR INVASIVE SPECIES: A CASE STUDY OF THE
LIONFISHES
Risk assessment is a useful tool employed to identify species that present
invasion risk and serves as a decision-support tool for potential management action.
However, predicting risk involves inherent uncertainty that can manifest from data
availability, assessor bias, and methodology (Orr 2003). The available data must
provide enough information about the biology and ecology of the species to satisfy the
requirements of the risk screening tool. Typically, species introductions go undetected
or do not receive scientific attention until populations have become relatively abundant
or until there is a perceived impact on the invaded system (Crooks 2005). One
exception to this general trend is when the species is important to fisheries,
aquaculture, or other human use. This can result in a paucity of quality data sources for
species that lack invasion history or species that have established incipient populations,
potentially hindering the ability of risk assessors to identify problematic taxa. As such,
uncertainty in risk assessment is often the consequence of lacking data (Orr 2003;
Mcgeoch et al. 2012).
The management of non-natives is primarily reactive, where mitigating action is
implemented post-establishment following documented spread and perceived impact
(Seastedt et al. 2008; Peters and Lodge 2009). This reactive approach relies on control
methods to reduce or prevent spread, which can be cost prohibitive, requiring sustained
management efforts (Leung et al. 2002), or on a “do nothing” approach where impacts
of species invasions are accepted as a social cost (Simberloff and Gibbons 2004). Due
to the difficulty of controlling invasive species following introduction, proactive
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management is receiving greater attention because it can be used to identify potentially
invasive taxa before they become established (e.g. horizon scanning, Roy et al. 2014).
Horizon scanning is a useful approach to invasive species management, but often
results in a large list of potential invaders and requires immense effort and expertise to
generate. Unfortunately, species identified during horizon scanning may also require
further evaluation before management decisions are made. Because invasion history is
a strong predictor of invasion success (Hayes and Barry 2008), a simpler alternative is
to evaluate species with demonstrated invasion history and their close relatives,
especially those with a known pathway of delivery for potential propagules to the region
of concern, thus narrowing the list of potential invaders to a practical size.
One group that meets both the criteria of previous invasion history and a direct
pathway for potential introduction into suitable habitat is subfamily of the lionfishes,
Pteroinae. The two invaders Pterois volitans and P. miles, henceforth referred to as the
invasive lionfish complex, have spread from South Florida northward along the Eastern
U.S. coastline, throughout the Greater Caribbean, Gulf of Mexico, and as far south as
Brazil (Schofield 2010; Ferreira et al. 2015). More recently, P. miles has established in
the Mediterranean as a lessepsian migrant through the Suez Canal (Bariche et al. 2017)
and continues to expand (Kletou et al. 2016; Azzurro et al. 2017). Regional control of
the invasive complex in the Atlantic Ocean and Gulf of Mexico is largely ineffective due
to larval replenishment and requires repeated culling efforts (Andradi-Brown et al. 2017;
Barbour et al. 2011; Dahl et al. 2016), although there may be some success on a
localized scale (Frazer et al. 2012; Green et al. 2017), suggesting proactive
management for these species and their close relatives may be appropriate.
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In addition to the invasive complex, several other lionfishes are imported into the
U.S. to supply the ornamental fish trade (ANSTF 2014). Due to their presence in the
pathway (Chapter 3), there is potential for the introduction of additional species of
Pteroinae through hobbyist release, a documented source of introduced marine fishes
(Semmens et al. 2004). Because the invasive complex exhibits a history of invasion in
the Atlantic basin and P. miles in the Mediterranean Sea, proactive investigation into the
risk of introduction, establishment, and the consequences of establishment for closely
related species of lionfishes is practical and timely. However, the application of risk
screening tools requires an understanding of potential errors arising from the quantity
and quality of data inputs. Despite potential false positives, well-informed risk screening
processes provide an effective alternative to post-spread impact mitigation (e.g. Keller
et al. 2007).
Here I explore how the availability of data, and hence uncertainty, changes
temporally throughout the invasion process by using the lionfish invasion as a case
study. I conducted a standardized literature review of 18 species in the genera Pterois,
Dendrochirus, and Parapterois to (1) characterize the volume and composition of
literature addressing the invasive complex pre-establishment and pre-spread, and drew
comparisons to literature developed post-spread and impact, (2) determine how the
volume and composition of literature addressing other members of Pteroinae compared
to the invasive complex, and (3) evaluate the quality of data addressing the Pteroinae
by characterizing the literature used to generate biological profiles of individual species
as part of a risk screening protocol.
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Methods
Data were obtained and characterized from two separate processes. First, a
standardized search was performed using the Web of Science database to access
literature and draw comparisons temporally and across species in a standardized
format. Second, broader non-standardized searches were conducted to obtain
additional literature from both primary and gray literature, which was used to develop a
comprehensive biological profile report on individual species (Lyons et al. 2017a).
Standardized Literature Review
I conducted a standardized literature review using the online database Web of
Science (available: https://webofknowledge.com) to identify the volume and types of
available data for 18 species in the subfamily Pteroinae. Searches were conducted in
November and December of 2017, and included literature published from 1900-2017.
Searches comprised one to five search terms per species. Search terms included the
combined genus and species name, known taxonomic synonyms, and accepted
common names. Queries for species lacking an English common name were restricted
to the scientific name of that species, such as in Pterois paucispinula (Matsunuma and
Motomura 2015). To appear in the search, articles needed to contain at least one
search term in the title, abstract, or keywords. Articles that satisfied the search criteria of
more than one species were counted multiple times, once for each species addressed.
Articles that did not contain any original data on the target species were excluded from
analysis.
In addition to the selection criteria defined above, the Web of Science journal
selection criteria requires that a journal must have been publishing for at least three
years. Journals are also evaluated based on the following criteria: timeliness (issues
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must be delivered on a regular schedule), use of international editorial conventions, full-
text English (or English bibliographic text), peer review process, editorial content,
international diversity (articles should include authors and editors from around the
world), and citation analysis. As such, this standardized literature search does not
capture the entirety of peer-reviewed literature from 1900-2017, but is a representative
distribution that is useful in identifying data gaps for potentially problematic invaders.
The literature addressing P. volitans/P. miles was separated temporally into three
periods to examine differences in the quantity and content of literature available pre-
introduction, post-introduction up until the first evaluation of the complex in its invaded
range, and from first evaluation to the present. The first period addresses pre-
introduction literature from 1900-1985, when the first occurrence of P. volitans was
reported in Dania Beach, Florida (Morris and Akins 2009). The second period contains
articles from 1986-2002, when the first study conducted in the invaded range was
published (Whitfield et al. 2002). The most recent period addresses articles published
from 2003-2017 and captures population increase and spread (see Schofield 2010).
Bioprofiles
I identified and categorized primary and gray literature using several libraries and
online databases, as well as expert opinion in the formulation of a comprehensive
biological profile report of the subfamily Pteroinae (Lyons et al. 2017a). Biological
profiles follow an established format used by the Florida Fish and Wildlife Conservation
Commission in previous risk assessments (Enge 2006; Hill 2013, 2014). Biological
profiles are designed to be used as a supporting document to inform risk screening
tools such as the Aquatic Species Invasiveness Screening Kit (Copp et al. 2016) or
comprehensive risk assessments (e.g. Hardin and Hill 2012). Major sections focus on
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the classification, distribution, biology, control, and potential impacts of each species.
Common names follow those reported in the National Invasive Lionfish Prevention and
Management Plan (ANSTF 2014). Reference backtracking was one of the primary
methods used to identify other relevant works. Books, reports, and other non-primary
sources were used in areas when peer-reviewed literature was lacking. Where
necessary, hobbyist literature (e.g. hobbyist discussion forums, hobbyist magazines,
and personal blogs) was used. These types of literature are less reliable, but can
provide information that is not addressed in primary literature. References to methods
used in the biological profile report (e.g. the use of climate matching models) were
excluded from this analysis because they did not contain any original data pertaining to
the Pteroinae.
Characterizing Literature
Articles from the standardized searches and biological profiles were separately
synthesized and categorized based on 1) the location where the study was conducted
or the source of specimens, 2) the category of the literature, and 3) the content category
of the article. Study location or source of specimen characterization includes a
distinction between studies conducted in the native range or specimens sourced from
native populations; studies conducted in the invaded range or specimens sourced from
the invaded range; or studies conducted in both the native and invaded range or a
comparison of specimens from native and invaded ranges. Literature type was
classified into six categories, including 1) peer-reviewed literature, 2) books, 3) reports,
technical papers, theses/dissertations, and symposia proceedings, 4) magazine and
newspaper articles, newsletters, online blogs, and aquarium literature, 5) online
databases, and 6) laws pertaining to the subfamily Pteroinae.
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Evaluation of an article’s content included 11 possible categories. Following the
methods described in a previous literature review of non-native fishes in Florida
(Schofield and Loftus, 2015), articles satisfying the requirements for more than one
category were included multiple times for a single species as a unique data point.
Content categories were adapted from a previous review (Schofield and Loftus, 2015) to
increase applicability to marine vertebrates and included 1) taxonomy and systematics,
2) origin, pathways, and spread in the introduced range, 3) distribution in the native
range, 4) habitat and tolerances, 5) life history, 6) diet, 7) health, 8) interspecific
interactions, 9) intraspecific interactions, 10) management, and 11) human health
(Table 2-1). Predation not explicitly measured to the species level, or studies that
measure the effects of predation to understand ecological interactions between
lionfishes and their prey were included in category 8) interspecific interactions.
Descriptions of study sites and the number of individuals collected for study were
excluded from category 2) origin, pathways, and spread in the introduced range.
Results
Standardized Literature Review
The standardized literature search yielded 284 articles across 18 species in the
subfamily Pteroinae, generating a total of 451 data points. Of those, 259 articles
addressed the invasive complex in its native or invaded range, comprising 91.1% of
total data points. The remaining 25 articles addressed 15 additional species and
accounted for 8.9% of total data points (Figure 2-1). Of the 259 total articles evaluated
for the invasive complex, 210 described research conducted in the invaded range
(81.1%), 36 studies were conducted in the native range (13.9%), and 13 studies
compared populations in native and invaded ranges (5.0%).
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There are no reported incidences of introduction or establishment for any
Pteroinae species outside the P. volitans/P. miles complex. As such, all studies were
conducted in either the native range or on fish sourced from the native range. Of the 25
articles returned, 56% addressed just three species: P. antennata, D. brachypterus, and
D. zebra (Figure 2-1). Over half the articles returned for species outside the invasive
complex were published in the last four years (Figure 2-2). Of the genera evaluated,
Parapterois had the fewest number of publications, comprising just 8% of total articles
returned for non-invasive lionfish. Hawaiian endemic species P. sphex and D. barberi
had zero publications. Similarly, searches for D. biocellatus returned zero publications.
Of the 40 data points, 22.5% fell into category 1) taxonomy and systematics, 22.5% into
category 3) distribution in the native range, 2.5% into category 4) habitat and
tolerances, 10% into category 5) life history, 5% into category 6) diet, 10% into category
8) interspecific interaction, 12.5% into category 9) intraspecific interaction, and 15% into
category 11) human health (Table 2-2). Zero articles addressed category 2) origin,
pathways, and spread in the introduced range, 7) health, or 10) management (Table 2-
2).
The volume and composition of literature addressing P. volitans/P. miles varied
temporally across the three periods—pre-introduction, introduction to first published
study in the invaded range, and spread in the tropical western Atlantic. From 1900-
1985, only three articles were returned, all of which fell into category 11) human health,
addressing venom chemistry, its physiological effects, or delivery mechanisms (Table 2-
3). During 1986-2002, 12 articles were returned, comprising 15 data points. Of these,
13.3% fell into category 1) taxonomy and systematics, 40% into category 11) human
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health, and the remaining 46.7% into categories 2-9 relating to biological characteristics,
ecological interactions, or distribution (Table 2-3). None of the articles published during
this period addressed category 6) diet, 7) health, 9) intraspecific interaction, or 10)
management. The most recent period from 2003-2017 contained 244 articles with a
total of 393 data points. Of these, 6.1% fell into category 1) taxonomy and systematics,
4.3% into category 11) human health, and 80.1% into categories 2-9. The remaining
9.6% addressed category 10) management (Table 2-3).
Bioprofiles
A total of 201 articles comprising 286 data points were evaluated and used in the
formulation of biological profiles for species not included in the invasive complex (Figure
2-1). Of these, 43.4% originated from peer-reviewed literature, 30.8% from books,
14.3% from technical reports, theses/dissertations, or symposia proceedings, 5.9% from
laws regulating these species in Florida, 4.2% from online databases, and 1.4% from
aquarium literature or online blogs. The species that exhibited the lowest relative
percentage of useable peer-reviewed literature include D. biocellatus (26.1%), D. bellus
(28.6%), P. heterura (28.6%), D. barberi (30.0%), P. mombasae (30.4%), and P. sphex
(31.3%) (Table 2-4). By content, 23% of data points fell into category 1) taxonomy and
systematics, 25.1% into category 3) distribution in the native range, 23.3% into category
4) habitat and tolerance, 4.2% into category 5) life history, 4.9% into category 7) health,
8.4% into category 8) interspecific interaction, 3.8% into category 9) intraspecific
interaction, and 7.3% into category 10) management, regarding regulation of these
species in Florida. Zero articles provided information on category 6) diet, to the species
level by use of gut contents, stable isotope analysis, or DNA barcoding.
26
The biological profiles for the invasive complex included 167 articles and account
for 274 data points. In contrast to others in the subfamily, 84.5% of total data points
originated from peer-reviewed literature, with an additional 7.7% from technical reports,
theses/dissertations, or symposia proceedings (Table 2-4). The remaining 7.7%
originated from other sources. By content, 10.2% of data points fell into category 1)
taxonomy and systematics, 23.4% into category 2) origin, pathways, and spread in the
introduced range, 4.9% into category 3) distribution in the native range, 15.3% into
category 4) habitat and tolerance, 6.2% into category 5) life history, 7.3% into category
6) Diet, 4.0% into category 7) health, 18.2% into category 8) interspecific interaction,
1.5% into category 9) intraspecific interaction, 7.3% into category 10) management, and
1.8% into category 11) human health.
Discussion
This analysis reveals limitations in the quantity and content of literature for
lionfishes that do not exhibit an invasion history, and a stark contrast to an established
body of literature on two related invaders. Lionfishes without prior invasion history are
data poor, yet they are still regularly found in invasion pathways (Chapter 3). As such, it
is important to evaluate alternative sources of literature, with the caveat that these
sources of information may be of reduced quality in comparison to primary sources.
Literature used in biological profiling to support risk assessment for potentially invasive
species of lionfish is of reduced quality when compared to the intensive study of the
invasive complex, and often relies on books or reports that are not readily accessible. In
contrast, the invasive complex is well-studied, but most literature has been generated in
the last decade (Côté and Smith 2018). The observed lag time between detection and
study is critical for intervention. While early detection and rapid response efforts are
27
effective management tools for localized populations or for those in confined water
bodies, the spatial scale and connectivity of marine systems present challenges for the
eradication or control of invasive species, and management efforts often require more
detailed information on the biology and ecology of the invader. Much more research
effort has been directed towards the invasive complex in comparison to other non-native
fishes that have successfully established outside of their native ranges (Schofield and
Loftus 2015). Ultimately, evaluating a risky group of fishes based on previous invasion
history can provide a more direct proactive alternative to extensive horizon scanning
(Roy et al. 2014) and a more cost-effective alternative to reactive management.
Over half of the literature available for potentially invasive lionfishes addresses
three species D. zebra, D. brachypterus, and P. antennata. Most other species of
lionfishes returned one or zero articles. Because the subfamily Pteroinae does not
include any major sportfish, does not make up a large portion of commercial food
fisheries, and is not found in aquaculture, it has received little research. When lionfishes
appear in fishing trawls, they are typically discarded as bycatch (Gibinkumar et al. 2012;
Sambandamoorthy et al. 2015); however, they are captured in some subsistence
fisheries (Poss 1999). Additionally, most lionfish are cryptic and difficult to detect in
underwater visual censuses (Kulbicki et al. 2012). As a result, abundance estimates are
often absent from non-targeted population surveys. Some of these lionfishes are traded
as aquarium specimens, resulting in much of the knowledge about this group residing in
hobbyist literature and other gray sources.
The extensive study of an invader typically occurs post-establishment (Crooks
2005), making high quality data inputs unavailable during the risk screening phase
28
(Sikder et al. 2006). Such conditions are characteristic of pre-invasion periods and the
early stages of invasions, resulting in uncertainty under conventional management
frameworks (Liu et al. 2011). The largest data gaps for potentially invasive lionfishes
occur in diet, life history, and interspecific interaction, which are critical elements for
estimating potential impacts. The only species of lionfish outside of the invasive
complex with food prey items identified to the species level was D. zebra (Moyer and
Zaiser 1981; Rizzari and Lönnstedt 2014). The diets of some additional lionfishes were
reported, but to the prey family or genus level (Harmelin-Vivien and Bouchon 1976).
Early diet studies relied exclusively on gut content analysis, making it difficult to identify
prey to the species level, and potentially introduce bias by excluding prey items that are
quickly digested (Dahl et al. 2017). Reproduction is reported in just two species, D.
zebra and D. brachypterus (Fishelson 1978; Moyer and Zaiser 1981). I propose an
increase in research effort for these species based on the group’s invasion history and
presence in the marine ornamental pathway.
The quality of literature on potentially invasive lionfish is reduced because it
relies on alternative sources of information. For example, many of the books that
address basic depth ranges or substrate preferences are field identification guides that
provide very limited information across a wide range of fish taxa, and the source for the
reported information is anecdotal or absent (e.g. Eschmeyer 1986; Allen and Erdmann
2012). Additionally, many non-primary sources are descriptive in nature, and do not
provide the quantitative measurements required to make comparisons across the
subfamily. Despite these limitations, the inclusion of non-primary literature filled some
data gaps that were not addressed by the peer-reviewed literature (Lyons et al. 2017a),
29
and doing so improves the resolution of biological and ecological characteristics that
can be used to inform risk screening.
In total, returned literature for all lionfishes outside the invasive complex
comprised less than 10% of what has been published on the invasive complex, which is
arguably one of the most intensively studied invasive fishes to date (Schofield and
Loftus 2015). However, some questions remain regarding life history (e.g. the presence
of ontogenetic shifts), diet (e.g. the importance of invertebrates), interspecific
interactions (e.g. predator recognition mechanisms in native prey fishes), and
intraspecific interaction (e.g. density dependent effects on spread and recruitment), all
of which are crucial to understanding the lionfish invasion in the western Atlantic (Côté
and Smith 2018). The invasive complex has seen a considerable shift from early
descriptive studies that serve as a literary foundation to manipulative studies that more
closely examine the invasion process (Schofield and Loftus 2015), which will likely aid in
future control efforts directed towards the invasive complex.
Despite their popularity in the marine aquarium trade (Rhyne et al. 2012; Lyons
et al. 2017b), biological data prior to introduction and during early spread of the invasive
complex are scarce (Côté and Smith 2018). In contrast, research effort post-spread has
resulted in a large body of literature on many aspects of biology and ecology, and has
even generated limited interest in the rest of the subfamily (Figure 2-1). Several studies
have utilized stable isotope analysis and DNA barcoding to accurately identify prey to
the species level (Côté et al. 2017; Muñoz et al. 2011; Valdez-Moreno et al. 2012).
Habitat use is well-studied in the invaded range (Biggs and Olden 2011; Claydon et al.
2012; Andradi-Brown et al. 2017). Life history is described in detail (Ahrenholz and
30
Morris 2010; Morris et al. 2011). However, this abundance of information was generated
largely in the last decade. Prior to introduction there is a paucity of literature addressing
basic biology and ecology. There is a 17-year lag period between the first peer-
reviewed article reporting occurrence and spread in the invaded range (Whitfield et al.
2002). Early detection initiatives in regions at the boundary of the invasion front began
in 2008, over two decades after introduction (Morris and Whitfield 2009; ANSTF 2014),
greatly reducing the likelihood of eradication. The occurrence of literature for the
invasive complex parallels two lag phases in the invasion process- one between first
introduction and first spread, and the second between first spread or early
establishment and marked increase in population growth (Kowarik 1995), suggesting
that the increase in knowledge of the invasive complex is a function of population
spread and perceived impact. If other species of lionfish were to successfully establish
and spread, the manipulative studies required to inform effective management would
not be possible in the absence of basic biological and ecological studies, and rapid
response efforts may be similarly delayed.
Early detection and rapid response provides opportunity for eradication or control
of spread during early establishment (Allendorf and Lundquist 2003; Vander Zanden et
al. 2010; Simberloff et al. 2013). Similarly, effective detection and response programs
provide the opportunity to study the basic characteristics of the invader where those
data are lacking. Some have stressed the utility of eradicating incipient populations
despite the amount of research conducted on the invader (Simberloff 2003). While this
strategy is effective for localized or isolated populations, marine invasions are subject to
larger and more dispersed spatial scales that offer opportunity for the broad dispersal of
31
propagules, making eradication or effective control more difficult. I propose that effective
monitoring and removal programs in marine systems would benefit from a basic
understanding of the life characteristics of the invader regarding habitat use and
dispersal mechanisms, which can be achieved in concert with rapid removal efforts. For
example, the spread of Caulerpa taxifolia in the Mediterranean (Meinesz et al. 2001)
was largely the result of inaction by managing agencies while preliminary studies on
biology and ecology were underway (Simberloff 2003). In contrast, the successful
eradication of C. taxifolia in southern California in 2005 was aided by prior knowledge
gained from its Mediterranean invasion that provided insight into potential dispersal
mechanisms and control methods, in addition to legislation passed to reduce the
probability of future introductions into the state (Anderson 2005). The continued
development of broad-scale habitat monitoring will be crucial for detecting non-native
fishes, especially for species that display cryptic behavior and those in expansive or
remote environments. Broad-scale monitoring should include the integration of citizen
scientists into early detection networks and the collation of data into easily accessible
public databases (Crall et al. 2010), as well as the development of new detection tools
such as the use of environmental DNA (eDNA) (Lodge et al. 2012).
Uncertainty in the systematics and taxonomy of lionfishes reduces the
reliability of the literature. The focus on systematics and taxonomy could be the result of
taxonomic instability in the subfamily and suggests that existing research on the
subfamily is in its infancy. Multiple studies have found polyphyly in the genera Pterois
and Dendrochirus (Kochzius et al. 2003; Freshwater et al. 2009). Several cryptic
species have been identified and described in the last 10 years, including D. hemprichi
32
(Matsunuma et al. 2017), D. tuamotuensis (Matsunuma and Motomura 2013), P.
andover (Allen and Erdmann 2008), P. cincta (Matsunuma and Motomura 2016), and P.
paucispinula (Matsunuma and Motomura 2015). Species ranges which were formerly
broad have been carved into smaller regions (e.g. Matsunuma and Motomura 2016),
resulting in literature that incorporates multiple congeners into a common data set.
Recently, genetic evidence has suggested hybridization in the native range between P.
russelii and P. miles, further confounding taxonomic relationships and including the
potential for heterosis in populations of the four largest species of lionfishes P. volitans,
P. miles, P. russelii, and P. lunulata (Wilcox et al. 2018). Differentiation of lionfish
species is important for risk assessment because of potential interspecific variation in
traits that may influence invasiveness. Additionally, taxonomic confusion presents an
added challenge to monitoring the volume and composition of lionfishes in the
ornamental pathway and the enforcement of regulation.
Risk assessment and invasive species prevention involves inherent uncertainty
where data are lacking (Sikder et al. 2006), but effective management requires rapid
action. The result is management decisions based on limited empirical data and expert
judgement applied across a wide range of competing societal values and objectives (Liu
et al. 2011). By implementing risk screens on groups (subgenus through family) that
have members with previous invasion history, the list of potential invaders that
traditional horizon scanning generates can be reduced, while still providing a useful
proactive framework to inform management action. I have taken this approach with
potentially invasive lionfishes and recommend extending this approach to other taxa,
terrestrial as well as aquatic, which have members with invasion history and similar
33
relatives in potential pathways of introduction. Early detection and rapid response
should remain a top priority, but researchers and managers should not overlook the
importance of gathering data on species that are detected. Where eradication is
unsuccessful, these data may inform control efforts to mitigate impacts. Ultimately, I
recommend an evaluation of species occurrence in introduction pathways and the
application of risk screening protocols to the Pteroinae. The identification of major data
gaps, the inclusion of new research to fill those gaps, and an understanding of existing
data limitations will provide a more informed process for the proactive management of
non-native species.
34
Table 2-1. Criteria for 11 content categories characteristic of the body of literature on the subfamily Pteroinae.
Category Criteria
1) Taxonomy and Systematics (Tax)
Species descriptions, species re-descriptions, taxonomic clarification, evolutionary history involving the use of morphological characters or genetic markers, descriptions of genetic and phenotypic characteristics.
2) Origin, Pathways, and Spread in Introduced Range (Path)
Origin of introduced populations, mechanisms of introduction, rate and direction of spread, relative and absolute abundances in the introduced range, spatial expansion/contraction of populations, records of first occurrence, and populations dynamics. Does not include articles that specify study location but are not a record of first occurrence.
3) Distribution in The Native Range (Natdis)
Spatial distribution in the native range, relative and absolute abundances in the native range, population expansion or contraction in the native range.
4) Habitat and Tolerance (Hab)
Substrate preference, association with structure, thermal niche, depth range, tolerance to changes in pH, dissolved oxygen, and salinity.
5) Life History (Lfhst) Reproduction, fecundity, early life history, age and growth.
6) Diet (Diet) Studies of prey composition by use of gut content, stable isotope, or DNA barcoding.
7) Health (Hlth) Susceptibility to external and internal parasites, viral or bacterial infections, and environmental contaminants.
8) Interspecific Interactions (Inter)
Behavioral and ecological interactions between two or more species, including predation, excluding parasitic interaction.
9) Intraspecific Interactions (Intra)
Aggression within species, courtship behavior, feeding interaction (including cooperative hunting and cannibalism), intraspecific density dependence, social behavior within a species.
10) Management (Mgmt) Control methods and efficacy, risk assessment and mitigation, impact management, modelling culling-based control and impacts, public perceptions related to management, economic valuation of the species.
11) Human Health (Hum) Venom composition, venom delivery apparatuses, effects of envenomation on human health, susceptibility to poisoning by consumption.
Categories were adapted from a previous literature review for freshwater non-native fishes (Schofield and Loftus 2015).
35
Table 2-2. Frequency of data points and respective category codes returned from a standardized literature search for 18 species of lionfish using the Web of Science Database.
Content Code
Species Tax Path Natdist Hab Lfhst Diet Hlth Inter Intra Mgmt Hum Total
P. volitans 15 88 2 48 23 19 13 62 7 33 24 334
P. miles 11 24 3 11 5 1 3 10 2 5 2 77
D. zebra 1 0 0 0 1 2 0 3 3 0 1 11
D. brachypterus 1 0 1 0 3 0 0 0 2 0 0 7
P. antennata 1 0 0 0 0 0 0 1 0 0 3 5
P. cincta 1 0 1 0 0 0 0 0 0 0 0 2
P. heterura 0 0 1 1 0 0 0 0 0 0 0 2
P. lunulata 0 0 0 0 0 0 0 0 0 0 2 2
P. macrura 1 0 1 0 0 0 0 0 0 0 0 2
P. mombasae 1 0 1 0 0 0 0 0 0 0 0 2
P. paucispinula 1 0 1 0 0 0 0 0 0 0 0 2
P. radiata 1 0 1 0 0 0 0 0 0 0 0 2
P. russelii 1 0 1 0 0 0 0 0 0 0 0 2
D. bellus 0 0 1 0 0 0 0 0 0 0 0 1
D. barberi 0 0 0 0 0 0 0 0 0 0 0 0
D. biocellatus 0 0 0 0 0 0 0 0 0 0 0 0
P. brevipectoralis 0 0 0 0 0 0 0 0 0 0 0 0
P. sphex 0 0 0 0 0 0 0 0 0 0 0 0 n = 451. Sampling period from 1900-2017. Tax = Taxonomy and Systematics; Path = Origin, pathways, and spread in the introduced range; Natdist = Distribution in the native range; Hab = Habitat and tolerance; Lfhst = Life history, Diet = Diet; Hlth = Health; Inter = Interspecific interactions; Intra = Intraspecific interactions; Mgmt = Management; Hum = Human health.
36
Table 2-3. Frequency of data points and respective category codes returned during a standardized search for the invasive complex P. volitans/P. miles prior to establishment, during the early invasion, and post-establishment, conducted using the Web of Science Database.
Content Code
Time Period Tax Path Natdist Hab Lfhst Diet Hlth Inter Intra Mgmt Hum Total
1900-1985 0 0 0 0 0 0 0 0 0 0 3 3
1986-2002 2 2 1 1 1 0 0 2 0 0 6 15
2003-2017 24 110 4 58 27 20 16 70 9 38 17 393 n = 411. Sampling period from 1900-2017.Tax = Taxonomy and Systematics; Path = Origin, pathways, and spread in the introduced range; Natdist = Distribution in the native range; Hab = Habitat and tolerance; Lfhst = Life history, Diet = Diet; Hlth = Health; Inter = Interspecific interactions; Intra = Intraspecific interactions; Mgmt = Management; Hum = Human health.
37
Table 2-4. Types of literature used in the formation of bioprofiles for 14 species of lionfish as part of a risk assessment for Florida.
Literature Type Species Pr Bo Te Aq Da La % Pr
P. volitans 149 9 14 2 1 1 84.7
P. miles 83 5 7 1 0 2 84.7
P. lunulata 14 1 2 0 1 2 70.0
P. radiata 21 7 5 0 2 2 56.8
D. brachypterus 16 10 5 0 1 0 50.0
P. antennata 14 10 2 0 1 1 50.0
P. russelii 14 11 3 0 1 2 45.2
D. zebra 15 13 4 0 1 2 42.9
P. sphex 5 4 4 0 1 2 31.3
P. mombasae 7 12 1 1 1 1 30.4
D. barberi 6 3 7 0 2 2 30.0
D. bellus 2 2 3 0 0 0 28.6
P. heterura 4 6 1 2 0 1 28.6
D. biocellatus 6 9 4 1 1 2 26.1 Pr = Primary literature; Bo = Book; Te = Technical paper, report, thesis/disseration, or symposia proceeding; Aq = Aquarium Literature, Magazine/newspaper articles, newsletters, online blogs; Da = Database; La = Law; % Pr = relative percentage of primary literature.
38
Figure 2-1. Number of articles and data points for 18 species of lionfish returned by
Web of Science during a standardized literature search (A) and number of articles and data points used in bioprofiles as a supporting document to risk assessment for the State of Florida (B). Bioprofiles for P. cincta, P. macrura, P. paucispinula, and P. brevipectoralis are combined with a close congener.
A
B
39
Figure 2-2. Frequency of articles published each year from 1900-2017 for the invasive
lionfish complex P. volitans/P. miles and for 16 other species of lionfish in the genera Pterois, Dendrochirus, and Parapterois. Dashed line indicates the first reported occurrence of the invasive complex in its introduced range. Dotted line indicates the first study of the invasive complex in its introduced range.
40
CHAPTER 3 CHARACTERIZING THE US TRADE IN LIONFISHES
The global trade in marine ornamental species encompasses over 1800 species
of fishes from at least 125 different families, including taxa from the small-bodied
Chromis viridis to the largest member of the family Labridae, the Humphead Wrasse
Cheilinus undulatus (Wabnitz et al. 2003; Rhyne et al. 2012). Among the species and
groups in trade is the ecologically and economically important group of venomous fishes
in the subfamily Pteroinae (Figure 3-1). The well-developed trade in marine ornamental
species supports collectors, wholesalers, and retailers economically, and can produce
conservation benefits through public exposure and outreach (Tlusty et al. 2013).
However, the global trade in these species is not without its drawbacks, including the
potential for introduction and establishment of non-native species (Holmberg et al.
2015), which can lead to economic, social, and ecological costs (Pimentel et al. 2005;
Lodge et al. 2006; Pejchar and Mooney 2009). Slowing or eliminating the spread of
introduced species post-establishment can be extremely difficult (Simberloff 2003).
Environmental damages and control programs for invasive marine and freshwater fishes
in the U.S. cost managers and stakeholders an estimated US$5.4 billion each year
(Pimentel et al. 2005). As such, it is important to evaluate the variety and volume of
potentially risky species in the marine ornamental trade to inform proactive
management approaches.
One such example of a marine invasion resulting directly from the global
aquarium trade is the invasive lionfish complex that includes Pterois volitans and P.
miles, which were introduced into the Atlantic Ocean in 1985 and have since spread
throughout the tropical western Atlantic Ocean, Gulf of Mexico, and Caribbean
41
(Schofield 2010). Pterois miles is now also spreading quickly through the
Mediterranean, as a Lessepsian migrant through the Suez Canal (Bariche et al. 2013;
Crocetta et al. 2015; Azzurro et al. 2017), further highlighting the invasion potential of
the subfamily. These two widespread invaders have documented impacts on ecosystem
structure and function throughout their invaded range (Albins and Hixon 2008; Albins
2013, 2015, Lesser and Slattery 2011). Because invasion history and propagule
pressure have a strong influence on the likelihood of establishment (Hayes and Barry
2008), and considering the large number of species in the global aquarium trade (Rhyne
et al. 2012), an appropriate proactive management approach focuses on evaluating risk
for groups such as the Pteroinae which have a history of invasion and associated
economic, social, and ecological costs.
Propagule pressure is often directly related to establishment probability (Hayes
and Barry 2008; Lockwood et al. 2009; Simberloff 2009; Briski et al. 2012) . Spatial and
temporal distribution, as well as the number and frequency of propagules greatly
influences the ability of an invader to overcome environmental and demographic
stochasticity and ultimately establish successfully (Shaffer 1987; Lande 1988;
Simberloff 2009). Although propagule pressure is an important predictor of
establishment, it is difficult to measure directly because data associated with the early
stages of invasion are often absent (Lockwood et al. 2009). Additionally, instances of
failed establishment typically go undocumented, impeding our ability to directly measure
the effects of propagule pressure (Johnston et al. 2009). As such, researchers utilize
surrogate measures to indirectly estimate propagule pressure, such as the movement of
visitors within nature reserves (McKinney 2002), shipping and boating traffic (Colautti et
42
al. 2003), or the movement of live marine fishes in the ornamental aquarium trade
(Semmens et al. 2004).
Marine introductions originating from the aquarium trade are historically rare but
are increasingly documented (Schofield et al. 2009). In Florida (USA) alone, at least 36
marine non-native fishes have been introduced by deliberate or unintentional release
across various pathways (USGS NAS 2018), with many of these introductions occurring
through hobbyist release (Semmens et al. 2004). For example, the Panther Grouper
Chromileptes altivelis has been reported from several locations in the Atlantic and Gulf
of Mexico, but is not thought to have established (Johnston and Purkis 2013). While few
introductions originating from the marine aquarium trade have resulted in establishment
and spread, two notable exceptions have had major consequences. First, the State of
California (USA) has spent considerable time and resources to eradicate the marine
algae Caulerpa taxifolia and prevent future establishment (Anderson 2005). Second, the
spread of the invasive lionfish complex in the western Atlantic Ocean has led to
reductions in native species abundance, diversity, and recruitment success (Albins and
Hixon 2008; Albins 2015). While it is not especially common, some marine fishes have
successfully established and spread through alternative pathways. The Regal
Demoiselle Neopomacentrus cyanomos has established populations in the Gulf of
Mexico by traveling on oil platforms, though the impacts of its spread are currently
unknown (Johnston and Akins 2016).
In previous studies, trade data were gathered on the ornamental industry in
aggregate (Smith et al. 2008) or on large groups of organisms such as marine
ornamental invertebrates (Rhyne et al. 2009) and marine ornamental fishes (Rhyne et
43
al. 2012). While this information is useful in identifying broad industry trends, a targeted
approach which examines trade in potentially risky groups based on previous invasion
history of close relatives may be more beneficial in the context of marine invasions
(Chapter 2), especially given the long list of traded species. Pterois volitans was once
the 29th most frequently traded marine fish by volume (Rhyne et al. 2012), which may
have contributed to elevated propagule pressure and thus a greater chance for
establishment; however, the volume of other lionfishes in the genera Pterois,
Dendrochirus, Parapterois, Brachypterois, and Ebosia have not been evaluated in
detail. To address discrepancies between the composition and volume of fishes arriving
in the U.S. and the composition and volume of fishes reaching the end of the trade
pathway, it is useful to also consider trade at the retail level in addition to import data, by
conducting surveys in coastal states with climatic conditions conducive to propagule
survival.
Here I characterize the ornamental introduction pathway of the subfamily
Pteroinae in the United States. Our goal was to identify the taxonomic composition and
volume of traded lionfishes, their collection origin, the major receiving ports, and their
occurrence in retail outlets. Importation was investigated using import records from the
U.S. Fish and Wildlife Service Law Enforcement Management Information System
(LEMIS) database, a central repository used to record wildlife arriving in the United
States. These data were supplemented by two domestic databases to capture the
collection and trade of the invasive complex from its invaded range, and two species of
lionfishes endemic to Hawaii, which are not reported under the LEMIS system. In
addition, I conducted a survey of lionfish availability in retail aquarium stores within ten
44
coastal states with access to potentially suitable marine habitat, as a comparative
measure to import records. This information on potential invasion pathways can be
especially useful when paired with rapid risk screening protocols to identify risky species
that are present in high volume.
Methods
While efforts are underway to increase the number of species in captive
production (Olivotto et al. 2011), the trade in marine ornamental fishes is supplied
primarily by the capture and transport of wild organisms (Wabnitz et al. 2003). To date,
there are no reports of captive culture for any species in the subfamily Pteroinae. As
such, all specimens are collected from their native ranges, or from invaded ranges in
the case of P. volitans and P. miles. Nine species of lionfishes are collected from ranges
throughout the Indo-Pacific, and two species of lionfishes are collected from their
endemic range in Hawaii (USA). All lionfishes are shipped to the United States via air
transport. The trade pathway from collector to hobbyist is characterized by a complex
chain of custody that presents some challenges to traceability and monitoring efforts
(Cohen et al. 2013), but typically includes consolidation at foreign export facilities,
departure from foreign exporter, arrival at domestic importer, dispersal from importer to
wholesaler, and dispersal from wholesaler to retailer (Zajicek et al. 2009; Cohen et al.
2013). However, the escape or intentional release of specimens during transport and at
points of consolidation is unlikely because of packaging practices and standards
(Zajicek et al. 2009). The risk of escape or release is highly concentrated at the end
user of the pathway, at the hobbyist level (Zajicek et al. 2009). Although the
establishment of marine invaders is uncommon, the invasive lionfish complex in the
western Atlantic is likely the result of hobbyist release (Whitfield et al. 2002).
45
Data Collection
The LEMIS database was accessed through a Freedom of Information Act
(FOIA) request for data from April 2, 2016 through April 1, 2017. The LEMIS database
gathers and combines electronically submitted and manually entered USFWS 3-177
forms (Declaration for Importation or Exportation of Fish or Wildlife) required by the
Code of Federal Regulations (CFR) title 50 part 14 (U.S. Office of The Federal Register,
1980). Relevant fields in the requested Standard Declaration Report include
identification of imported lionfishes to the species level, quantities of imported lionfishes,
the foreign country of origin, the foreign country of export, and the domestic receiving
port. Additional proprietary information is collected, but redacted prior to fulfilling a FOIA
request. Only records with the wildlife designation indicating that the shipment was
comprised of live individuals (LIV) were included in the analysis. An additional 3,351
lionfish were excluded from the analysis because they were imported as preserved
specimens (SPE) or jewelry (JWL).
Because the LEMIS database applies only to trade originating from outside the
United States, it does not report domestic collection or transport of lionfishes. I included
the collection and trade of the invasive complex P. volitans/P.miles in Florida (the
primary collection site for the invasive population) using the Florida Fish and Wildlife
Conservation Commission Fish and Wildlife Research Institute’s Annual Commercial
Fishery Landings database (FFWCC FWRI 2017). This database includes the county of
collection, the quantity of lionfish collected, the number of commercial trips taken, and
the value of collected lionfish. Reporting is gathered from trip-ticket requirements for
commercial landings (Florida Statute 370.07.6.a, 1997). The volume of P. volitans
sourced from other countries in the invaded range and from adjacent U.S. states is
46
likely low, but may increase these numbers slightly. Additionally, I included the trade of
Pterois sphex and Dendrochirus barberi, two Hawaiian endemic species of lionfishes,
by submittal of a Request for Commercial Fishing Report Information to the Hawaiian
Division of Aquatic Resources (DAR). This database includes time of harvest, quantity,
and value of lionfishes collected from commercial fishing (Hawaii Revised Statute 189-
3, 2015).
Retail Surveys
The occurrence of lionfishes in 168 retail stores within ten coastal U.S. states
was evaluated during a two-week period from June 29th to July 12th, 2017. States were
selected to reflect the distribution of the invasive lionfish complex in US waters, and
thus regions where warm climatic conditions are most likely to support the survival of
other species of lionfishes (Lyons et al. 2017). California was included because P.
volitans has a thermal niche that may allow for permanent established populations in
some areas of southern California (Dabruzzi et al. 2017), and because it is a major hub
for the marine ornamental fish trade (Williams et al. 2015). Retail stores were identified
and selected using a standardized Google search for the term “saltwater aquarium store
in” followed by the state where that store is located. To meet selection criteria, identified
retailers had to 1) sell live saltwater fishes, 2) maintain regular business hours (i.e.,
stores by appointment only were excluded), 3) sell directly to the public, and 4) have a
listed phone number. Retail stores were selected in the order that they appeared in the
search. The number of retail stores surveyed in each state was determined by that
state’s population reported by the 2010 United States Census Bureau, to reflect the
positive relationship between population size and the potential for introduction (Gertzen
et al. 2008; Strecker et al. 2011). California was assigned an arbitrary value of 50
47
representative stores because it has the largest population of any U.S. state. Texas
(34), Florida (26), Georgia (14), North Carolina (12), Virginia (10), South Carolina (6),
Alabama (6), Louisiana (6), and Mississippi (4) were assigned a representative number
of retail stores proportional to state population.
The survey used a standardized script format, in which the surveyor identified
themselves, the intent and purpose of the study, asked about species availability for all
species in the subfamily Pteroinae, and included the option to opt out of the survey.
Common names were verified with purchasing lists when available. Each available
species was recorded as a unique hit, where multiple individuals of the same species at
one location resulted in just one hit for that species. Stores unwilling to disclose stock
lists were recorded as non-participant. Stores with nonfunctional listed telephone
numbers, or those that did not answer the store’s listed telephone after three attempts
were recorded as not available (N/A). Both non-participant and N/A occurrences were
included in the total number of stores surveyed but were excluded from percent
occurrence to reflect uncertainty in species availability.
Results
Between April 2016 and April 2017, the U.S. ornamental marine fish market
imported 39,648 live Pteroinae of nine species. An additional 2,329 individuals were
collected from Florida, and 32 individuals were collected from Hawaii (Figure 3- 2).
Overall, 57.2% of live imports were in the genus Pterois, 42.7% in the genus
Dendrochirus, and just 0.03% in the genus Parapterois. The genera Brachypterois and
Ebosia were absent from the data sources. Of the 21,711 imported Pterois, 3.2% were
not identified to the species level. Of the 17,926 imported Dendrochirus, 4.8% were not
identified to the species level. Pterois volitans accounted for 40.2% of all lionfishes
48
imported, followed by Dendrochirus zebra which accounted for 31.5% of imports (Figure
3-2). Five species Dendrochirus brachypterus, Pterois antennata, Dendrochirus
biocellatus, Pterois radiata, and Pterois lunulata were traded in comparatively moderate
to low volumes, and three species were traded in very low volumes, including D. barberi
with just 32 individuals, Parapterois heterura with 11 individuals, and Pterois mombasae
with two individuals (Figure 3-2). Hawaiian export volume for P. sphex was unavailable
because only a single collector targeted that species from April 2016 to April 2017, and
therefore the data were redacted as proprietary.
Four countries accounted for 90.3% of the total number of lionfishes
collected including, in order of total quantity, Indonesia, Philippines, Kenya, and Sri
Lanka (Figure 3-3). An additional 9.1% of lionfishes were listed under the origin
designation various (VS), which denotes shipments of lionfishes sourced from multiple
countries. Two countries, Indonesia and Philippines, accounted for 71.8% of live lionfish
imports (Figure 3-3). The collection of P. volitans in Florida comprised only 12.3% of
total trade volume for this species (Figure 3-2). There were no noticeable trends in the
seasonal availability of lionfishes by species, but overall lionfish imports were highest in
April and May (Figure 3-4).
The port of Los Angeles received 74% of the lionfishes imported into the
U.S., followed by New York (8.6%), Chicago (7.7%), San Francisco (3.8%), and Miami
(2.9%) (Figure 3-3, Figure 3-5). Additional receiving ports included Dallas, Atlanta,
Detroit, Newark, Seattle, Minneapolis, and Orlando, but these ports in aggregate
accounted for only 2.9% of total imports (Figure 3-5). Of 1,156 lionfishes received by the
49
port of Miami, nearly 40% were not identified to the species level. On average, lionfish
imports included an average of 8.2 individuals.
I found that 75 of 168 (43.5%) retail shops had at least one species of
lionfish in stock (Figure 3-6). Another 44.6% did not have any lionfish on-site, 8.3% did
not answer the store telephone after three contact attempts or had a telephone that was
no longer in service, and 3.6% did not participate in the survey. Only six species of
lionfishes appeared in surveyed stores. P. volitans was present in 39.9% of surveyed
stores, while Dendrochirus brachypterus was present in 12.2%, D. zebra in 8.1%,
Pterois antennata in 2.7%, Pterois radiata in 2.0%, and Dendrochirus biocellatus in
2.0% of retail shops (Figure 3-6).
Discussion
I identified considerable variation in species diversity and volume at both the
import and retail level. The marine ornamental trade is a strong introduction pathway for
two species of lionfishes, but moderate to very weak for others (Figure 3-2). Lionfish
import is highly concentrated at the port of Los Angeles (Figure 3-5), and most
specimens originate from Philippines and Indonesia (Figure 3-3). Retail surveys
indicated a much more limited diversity of lionfishes than previously thought, especially
when compared to stock lists provided by online vendors (Figure 3-6). The genera
Ebosia and Brachypterois were entirely absent from trade at both the import and retail
level. Ultimately, these data indicate that there is substantial variation in the volume,
diversity, and destination of lionfishes in trade, suggesting that risk is not uniformly
distributed across the subfamily.
The relative volume of lionfish trade in the U.S. is low compared to many
other taxa. On an annual basis, lionfishes likely comprise a fraction of a percent of the
50
total volume of traded marine fishes. From 2004 to 2005, over 11 million marine fishes
were imported (Rhyne et al. 2012). However, more than half of that trade was
comprised of just 20 species (Rhyne et al. 2012). In some cases, a single species can
account for nearly 10% of total import volume (Rhyne et al. 2012). Despite high trade
volumes, none of these species have established populations outside of their native
ranges. The lack of establishment success further highlights the importance of species
characteristics in predicting risk, and the utility of characterizing the trade of species that
share common features with known invaders.
The diversity of lionfishes available directly to hobbyists is likely much lower than
previously thought. Many online retailers advertise and presumably sell a diverse stock
list of Pteroinae directly to the public, but that diversity was not apparent in our retail
survey results. For California, Williams et al. (2015) reported the online availability of 12
species to hobbyists from internet sources. At the retail level, our survey found only six
species available in 10 coastal states, only five of which were found in 50 Californian
retail stores. Additionally, the presence or absence of lionfishes in our survey was
verified with current stock lists, whereas previous surveys only reported the diversity of
lionfishes advertised online (ANSTF 2014; Williams et al. 2015). Lower species diversity
at the retail level is also supported by the LEMIS and Hawaiian DAR databases which
indicate the import of only 11 species of lionfishes, five of which were reported in
exceedingly low volumes (Figure 3-2). Retail surveys were conducted during a two-
week period with a representative sample size and therefore the retail trade was not
captured in its entirety. While lionfish import volume does vary somewhat on a temporal
51
basis with a peak in April and May, it does not contain any demonstrable trends by
species (Figure 3-4).
Although import volume is a direct measure of the total volume of lionfish
coming into the United States, other factors may influence true propagule pressure.
Body size is one of the most important factors affecting the probability that an individual
fish will be released because it can outgrow home aquaria (Holmberg et al. 2015).
There are considerable differences in maximum body size among the lionfishes. The
largest species of traded lionfishes P. volitans reaches 45.0 cm, over three times the
size of the smallest traded lionfish D. biocellatus (Table 3-1). Members of Pterois are on
average larger than members of Dendrochirus (Table 3-1). Many additional factors may
act as modifiers on propagule pressure (Strecker et al. 2011), including species
aggression, difficulty of care, a perceived danger to oneself or a family member (e.g.
venomous fishes), and economic distress or an inability to provide adequate housing.
Such modifiers are extremely difficult to quantify, but likely have some effect on the
potential of release.
Mortality during wholesaler consolidation and during transit from wholesaler to
retailer can vary considerably (Cohen et al. 2013) and may be higher for some species
of lionfishes (Lyons et al. 2017). Collection methods, holding conditions, and shipping
practices influence mortality rates across a range of marine taxa (Wabnitz et al. 2003;
Olivotto et al. 2011), which may have important implications for the diversity of species
available to consumers. The use of chemical anesthetics during collection can have a
major impact on the overall survival of specimens in trade (Vaz et al. 2017). Availability
to hobbyists will ultimately be influenced by this chain of events, and therefore trade
52
volume at the end of the pathway will be reduced. For example, despite a much higher
import volume of D. zebra, our results show that D. brachypterus is more often
encountered in retail settings (Figure 3-2, Figure 3-6). This might indicate that D.
brachypterus is more resilient to handling and transport, which affects how likely this
species will be encountered by the consumer.
One drawback of using import data as a surrogate for propagule pressure is that
it does not account for redistribution after fishes are received at the port of destination.
This is especially important for large countries like the United States, which exhibits
variation in suitable habitat and ultimately risk. Redistribution of lionfish likely plays an
important role during transport from wholesaler facilities to retail locations, affecting
availability to the consumer. For example, Los Angeles is a major shipping hub for
fishes originating from the Indo-Pacific and several major wholesalers are in proximity to
the ports so that incoming shipments of fish can be consolidated and quickly
redistributed to retail stores. The proximity of hobbyists to suitable habitat and the
transportability of the taxa will ultimately affect propagule pressure and the risk of
establishment (Williamson 1996). For example, habitat nearer to roads or footpaths
have a greater number of introduced fishes than those in remote locations (Copp et al.
2005). Similarly, thermal tolerance and climatic suitability influence the ability of
introduced fishes to establish permanent populations (Bomford et al. 2010). The broad
distribution of many lionfishes in the Indo-Pacific (Kulbicki et al. 2012), and
demonstrated cold-tolerance in some (Lyons et al. 2017), suggests that many species
have the potential to establish in the western Atlantic, Gulf of Mexico, and Caribbean. A
large fraction of imported lionfish will be redistributed to destinations which are located
53
far from suitable marine habitats. Therefore, an assessment of trade at the retail level is
useful because it identifies trade volume and spatial distribution at the end user
destination, where introduction is most likely to occur (Zajicek et al. 2009).
Lionfishes share many morphological characteristics (Figure 3-1), which may
provide opportunity for species misidentification. Sri Lanka and Kenya are not included
in the historical native range of P. volitans, yet the LEMIS database reports that P.
volitans comprises 92.9% of lionfish trade from Sri Lanka and 56.6% from Kenya
(Figure 3-3). This is suggestive of misidentification, where the closely related congeners
P. miles and P. russelii, species that are native to the Western Pacific and Indian
Ocean, are likely exported and traded as P. volitans. Misidentification of large bodied
Pterois is noteworthy given genetic evidence of hybridization in P. volitans (Wilcox et al.
2018), where future introductions of P. volitans, P. miles, P. russelii, and P. lunulata
may elevate the risk of hybrid vigor. Additionally, several ports received individuals that
were not identified to the species level. Over 40% of the 1,200 individuals received by
the port of Miami were not identified to the species level (Figure 3-3). These potential
errors in database reporting will ultimately affect the volume and diversity of lionfishes
that reach the consumer, which has important implications for the management and
traceability of the marine ornamental trade.
Import data are useful for evaluating the total trade volume of marine fishes
entering the United States. Combined with retail surveys to account for modifiers on
availability at previous stages in the pathway (Wabnitz et al. 2003; Olivotto et al. 2011;
Cohen et al. 2013), managers can better characterize the diversity of species at the end
of the pathway where release is most likely to occur (Semmens et al. 2004; Zajicek et
54
al. 2009). By identifying hardy species that occur in high trade volumes, understanding
spatial distribution at the import level, and spatial redistribution at the hobbyist level,
trade data can focus risk assessment and management towards species with high
propagule pressure, a consistent predictor of establishment success (Lockwood et al.
2009). Given previous invasion history in the Pteroinae and a strong pathway for some
species, future research should aim to apply proactive risk screening measures such as
the Aquatic Species Invasiveness Screening Kit to the subfamily (Copp et al. 2016). To
reduce the uncertainty of risk screens, data gaps should be identified, and future efforts
should be made to better understand their basic biology and ecology (Chapter 2).
55
Table 3-1. Maximum body size of Pterois, Dendrochirus, and Parapterois present in the U.S. ornamental aquarium trade.
Species Maximum size (TL) Reference
D. biocellatus 13.0 Kuiter and Tonozuka 2001
D. barberi* 16.5 Randall 1985
D. brachypterus 17.0 Lieske and Myers 1998
D. zebra 25.0 Myers 1991
P. mombasae 20.0 Kuiter and Tonozuka 2001
P. antennata 20.0 Eschmeyer 1986
P. sphex* 21.0 Randall 1985
P. radiata 24.0 Lieske and Myers 1998
P. russelii** 30.0 Sommer et al. 1996
P. miles** 35.0 Sommer et al. 1996
P. lunulata 35.0 Kuiter and Tonozuka 2001
P. volitans 45.0 Whitfield et al. 2007
P. heterura 38.0 Allen and Erdmann 2012 * denotes species reported by the Hawaiian Division of Aquatic Resources. ** denotes species that were not reported in any database but are likely collected and traded under a species misidentification.
56
Figure 3-1. Eight species of lionfishes present in the U.S. ornamental fish trade from
April 2016-2017. Genera Pterois (top) and Dendrochirus (bottom).
57
Figure 3-2. Total volume of each species of lionfish imported and recorded in the U.S.
Fish and Wildlife Service’s LEMIS database from April 2016-2017 (black bar). The red bar indicates lionfish collected in Florida (invaded range) and the green bar indicates lionfish collected from the Hawaiian Islands. Reported volume of D. barberi = 32, P. heterura = 11, P. mombasae = 2. The quantity of P. sphex was unavailable because a single commercial collector reported landings, therefore trade volume was redacted as proprietary by the Hawaiian Division of Aquatic Resources.
58
Figure 3-3. Species composition and relative volume of lionfish trade for six major
receiving ports (Los Angeles, New York, Chicago, San Francisco, Miami, and Dallas/Ft. Worth) accounting for 98.6% of all lionfish imports into the United States from April 1, 2017-2018 (A), and species composition and relative volume for five major collection origins (Indonesia, Philippines, Kenya, various, and Sri Lanka) accounting for 99.2% of all collections (B). Size of pie chart is proportional to total trade volume received by that port. The port of Los Angeles is reduced in scale by 856% to equal the area of the second largest port and accounts for 74.0% of all lionfish imports (n = 29,414). Ports that received lionfishes, but did not comprise more than 1% of total trade volume are included as additional points. Spp. represents lionfishes that were not identified to the species level. “Various” represents lionfishes that were sourced and collated from multiple countries.
A
B
59
Figure 3-4. Monthly variability for the top five species of lionfishes by import volume
from April 2, 2016 to April 1, 2017.
0
500
1000
1500
2000
2500
3000
3500
4000
4500
P. volitans
D. zebra
D. brachypterus
D. biocellatus
P. antennata
60
Figure 3-5. Total volume of lionfish received at ports in the United States between April
2, 2016-April 1, 2017 reported by the U.S. Fish and Wildlife Service LEMIS database (n = 39,648). Los Angeles = 74% of imported lionfish; New York = 8.6%; Chicago = 7.7%; San Francisco = 3.8%; Miami = 2.9%; Sum of all other ports = 2.9%.
61
Figure 3-6. Percent occurrence of six species of lionfish identified in U.S. retail
aquarium stores in 10 coastal states during a two-week survey from June 29-July 12, 2017. P. volitans = 39.9%; D. brachypterus = 12.2%; D. zebra = 8.1%; P. antennata = 2.7%; P. radiata = 2.0%; D. biocellatus = 2.0%. No other lionfish species were reported during retail surveys.
62
CHAPTER 4 RISK SCREEN OF LIONFISHES PTEROIS, DENDROCHIRUS, AND PARAPTEROIS
FOR COASTAL WATERS OF THE GULF AND ATLANTIC
The trade in marine ornamental fishes is diverse and includes over 1800 species
across 125 families (Rhyne et al. 2012). The United States is a leading importer of
marine life, and is the point of destination for over half of all marine ornamentals (Tissot
et al. 2010). This includes the lionfishes, which contains the invasive complex P.
volitans and P. miles in addition to several other regularly traded species (Chapter 3). If
managed with care, the marine ornamental trade has the potential to provide a
sustainable income throughout the supply chain, as well as contribute conservation
benefits through research initiatives and education at public aquariums (Tlusty et al.
2013). However, the aquarium trade is not without its drawbacks such as the release of
aquarium fishes into the environment (Semmens et al. 2004). With high diversity in the
marine ornamental industry, it is difficult to estimate invasion risk for even a fraction of
the taxa. Choosing where to expend resources on risk assessment is a daunting
question.
In comparison to freshwater fishes, few non-native marine ornamental fishes are
established, and fewer still have documented impacts on native fauna (Schofield et al.
2009; Schofield and Loftus 2015). The primary exception is the invasive lionfish
complex, Pterois volitans and Pterois miles, which is widely established in the western
Atlantic Ocean and Gulf of Mexico (Schofield 2010; Ferreira et al. 2015). Establishment
of the invasive complex in the western Atlantic is likely the result of aquarium release
(Whitfield et al. 2002). More recently P. miles has spread into the Mediterranean Sea
through the Suez Canal (Crocetta et al. 2015; Azzurro et al. 2017). In the Atlantic
Ocean, lionfish have a range of ecological, economic, and social impacts, many related
63
to direct and indirect consumptive effects on native reef organisms, reducing the
recruitment, richness, and abundance of economically important sport fishes (Albins
and Hixon 2008; Albins 2015), and potentially further degrading already pressured
coastal systems (Frazer et al. 2012). Characteristics contributing to invasion success
include predation defense, rapid growth and maturity, and high fecundity (Morris and
Akins 2009; Morris et al. 2011; Edwards et al. 2014). Several other lionfishes in the
genera Pterois, Dendrochirus, and Parapterois are traded (Chapter 3), many sharing
characteristics with the invasive complex (Chapter 2). For example, the lower lethal
temperature tolerances of D. zebra and D. brachypterus (Lyons et al. 2017) are similar
to that of P. volitans (Kimball et al. 2004; Dabruzzi et al. 2017). Because of their
presence in the ornamental pathway and shared characteristics with the invasive
lionfish complex, a closer evaluation of risk for the subfamily Pteroinae is warranted
(Chapter 2, 3).
One approach to proactive risk assessment is the use of rapid risk screening
tools to identify areas of risk for non-native species in potential introduction pathways,
especially for taxonomic groups that have already proven invasive (Chapter 2,3). Risk
screening can provide timely information related to the need for subsequent resource
allocation towards more comprehensive risk assessment for species of elevated
concern, which can ultimately influence management actions such as public outreach
initiatives or regulatory response (Copp et al. 2009; Hill et al. 2014).
Here I apply a relatively new tool, the Aquatic Species Invasiveness Screening
Kit (AS-ISK) (Copp et al. 2016) to 14 species of lionfishes in the genera Pterois,
Dendrochirus, and Parapterois for coastal waters of the State of Florida to 1) generate a
64
relative risk score for lionfishes by evaluating climate match, biological, and ecological
characteristics and 2) compare the score of those species to the two well-known
invaders, P. volitans and P. miles. This framework provides a transparent process which
illuminates data gaps, informs management, and serves as the basis for more
comprehensive risk assessment if warranted. Risk screening is appropriate for the
marine ornamental trade and the Pteroinae in particular because of the high diversity
and volume of data limited species in trade as well as the widespread establishment
and considerable impacts of two lionfishes. Application of risk assessment to marine
ornamental fishes can improve the sustainability of the trade by directing management
effort towards species or groups that pose an elevated invasion risk.
Methods
Assessments were conducted on 14 species of ornamental lionfish using AS-ISK
v1.3 (Copp et al. 2016), including the two known invaders P. volitans and P. miles.
Species were selected based on their 1) inclusion within the subfamily Pteroinae which
contains the invasive complex, 2) presence in the ornamental aquarium trade (Chapter
3), and 3) taxonomic standing. Recently described or re-described species were omitted
from the assessment because of the near complete lack of data on distribution, biology,
and ecology (Chapter 2), including D. hemprichi (Matsunuma et al. 2017), D.
tuamotuensis (Matsunuma and Motomura 2013), P. andover (Allen and Erdmann 2008),
P. cincta (Matsunuma and Motomura 2016), P. macrura (Matsunuma et al. 2013), and
P. paucispinula (Matsunuma and Motomura 2015). The genera Brachypterois and
Ebosia were omitted from the assessment because they did not occur in a recent
survey of the marine ornamental trade (Chapter 3). The risk assessment (RA) area for
this study was defined as the coastal waters surrounding the State of Florida. Selection
65
of the RA area was based on a historically high introduction of marine ornamental fishes
(Semmens et al. 2004; Schofield et al. 2009) and a dense coastal population in close
proximity to suitable estuarine and marine habitats. Additionally, lionfish were first
documented outside of their native range along the Florida coast (Schofield 2010).
The AS-ISK v1.3 is an adaptation of the Weed Risk Assessment (Pheloung et al.
1999) following the Fish Invasiveness Screening Kit (FISK) v1 (Copp et al. 2005, 2009)
and FISK v2 (Lawson et al. 2013). The tool follows the same premise that species with
an invasion history are more likely to become invasive in other regions that exhibit
similar climate and habitat characteristics (Copp 2013). The AS-ISK was developed as
a taxon-generic tool designed to replace existing taxon-specific screening tools (Copp et
al. 2016). Since its development, it has been tested on freshwater fishes in Turkey
(Tarkan et al. 2017), China (Li et al. 2017), and Bosnia and Croatia (Glamuzina et al.
2017). Only one marine fish application of AS-ISK is currently published, an assessment
of P. miles for the eastern Mediterranean Sea (Filiz et al. 2017).
The AS-ISK consists of 49 questions relating to the biological and ecological
characteristics of species, and characteristics of the RA area, grouped into two broad
categories on biogeographical and historical information, and biology and ecology
(Table A-1). The combined total for these two categories generates a basic risk
assessment (BRA) score ranging from -12 to 64, with a higher score indicating elevated
risk. An additional 6 questions address changes in invasion risk resulting from climate
change, generating a separate modified climate change assessment (CCA) score
ranging from -24 to 76 (Table A-1). Question scoring for the BRA and CCA is primarily
additive, but some questions act as response modifiers. Additionally, the tool provides
66
guidance for each question to improve clarity and reduce subjectivity associated with
varied assessor interpretation. Assessors answer questions using primary sources, gray
literature, and expert opinion where literature is absent, documenting justifications for
answers to increase transparency. A confidence factor (CF) was calculated separately
for the BRA and CCA score as:
∑(CQi)/(4 × n) (i = 1, …, n)
where CQi is the certainty for a given question, a score of 4 is the maximum achievable
value for certainty, and n is the number of questions in the assessment (Almeida et al.
2013; Puntila et al. 2013). Therefore, the CF for an assessment ranges from 0.25-1.
Questions related to climate suitability were addressed using Climatch (Bureau of
Rural Sciences 2009), a climate matching model that incorporates 16 climatic variables
gathered from coastal weather stations in the native range of the species and compares
those data to 67 coastal weather stations in Florida. Each station in the RA area
receives a climate matching score ranging from 1-10, depending on its similarity to
native range stations. A climate 6 proportion was calculated by dividing the number of
stations scoring ≥ 6 by the total number of stations (Bomford et al. 2010). A climate 6
proportion below 0.005 is a low climate match, a score greater than 0.103 is a high
climate match, and a score falling between these threshold values is a medium climate
match (Hoff 2016). Native ranges were determined using the Global Biodiversity
Information Facility (GBIF 2017) and an unpublished database provided by Robert
Myers (R. Myers, Coral Graphics, personal communication). Questions relating to
changes in invasion potential due to climate change used the Environmental Protection
67
Agencies Sea Surface Anomaly projections (EPA 2016) as a standard for global sea-
surface temperature change by all assessors.
Three assessors (TJL, QMT, and ADD) scored each species of lionfish
independently. Another project team member (JEH) independently reviewed all
assessor responses and justifications, identified potential areas of disagreement in
responses among assessors, and evaluated answers and justifications for errors.
Because AS-ISK is a recently developed tool, thresholds for low, medium, and high-risk
species have not been established for the RA area. As such, the present study assigns
scores to P. volitans and P. miles to represent two known invaders and provide context
to the scoring of other species of lionfishes specific to the RA area. Linear regression
was conducted on maximum reported body size and mean BRA score, as well as on
climate 6 proportion and mean BRA. All statistical analysis was conducted using
RStudio (R Core Team 2016).
Results
Mean BRA scores of potentially invasive lionfishes ranged from -0.3 for D. bellus
to 17.7 for P. russelii (Table 4-1, Figure 4-1). Mean CCA scores of potentially invasive
lionfishes had a wider range than the BRA, from -0.7 for P. heterura to 20.3 for P.
russelii (Figure 4-1). The invasive complex of P. volitans and P. miles had a mean BRA
across assessors of 34.0 and a mean CCA of 36.7 (Figure 4-1). The lowest individual
assessor score after CCA modification was a -4.0 for D. barberi, and the highest
individual assessor score after CCA modification was 39.0 for P. volitans and P. miles.
A lack of invasion history and tolerance attributes that decrease establishment and
persistence resulted in relatively low risk scores for many lionfish species (Figure 4-2).
The elevated risk scores of P. volitans and P. miles were largely driven by documented
68
invasion history (establishment and impacts) and traits that increase persistence, and
moderately by documented tolerance attributes, mechanisms of dispersal, reproductive
traits, and the potential for future climate change projections to increase the vulnerability
of the RA area or the magnitude of invader impacts (Figure 4-2). The mean risk score
for Pterois (not including P. volitans and P. miles) was 9.8 BRA (SD = 4.13) and 10.5
CCA (SD = 4.97), more than twice that of Dendrochirus which scored a mean of 4.9 (SD
= 4.64) for BRA and 4.9 (SD = 4.77) for CCA assessments. The BRA assessments had
a mean delta of 3.8 (SD = 2.33), ranging from 1 for P. mombasae to 11 for P. russelii
(Table 4-1). The CCA assessments had a mean delta of 4.4 (SD = 2.21) with a range of
2 for D. bellus, D. biocellatus, and P. antennata, to a delta of 10 for D. barberi.
Shared characteristics that increased risk scores included venomous spines
(Q4), a high number of propagules (Q3), young age at first reproduction (Q34),
proximity to protected areas (Q36), dispersal as both eggs and larvae within the RA
area (Q38-39), rapid dispersal in the RA area resulting from those life history
characteristics (Q42), and a lack of effective natural predators in the RA area (Q49).
Questions that reduced the risk score of many species of lionfishes included a lack of
domestication (Q1), no evidence of naturalized populations in the RA area (including the
invasive complex) (Q9), a lack of parental care (Q28), no evidence of hybridization with
native taxa (Q30), no evidence of hermaphroditism or asexual reproduction (Q31), no
means of attachment to hard substrates (Q37), no evidence of propagules being
dispersed by other taxa (Q41), no evidence of density dependent dispersal (Q43), and
no tolerances to desiccation (Q49). Sections that contain major differences in scoring
69
were largely limited to questions that related to undesirable traits and tolerance
attributes.
The average CF was 0.72 (SD = 0.04) for assessments conducted on the
invasive complex, and 0.59 (SD = 0.08) for assessments conducted on other potentially
invasive lionfishes (Table 4-1). Questions with the lowest average CF included those
addressing the introduction of non-native parasites or susceptibility to native parasites
(Q20-21), density dependent dispersal (Q43), tolerance attributes to changes in water
quality (Q45), effective control measures (Q46), and tolerance to human disturbances
(Q47).
The mean climate 6 proportion was 0.70 (SD = 0.39). The invasive complex P.
volitans and P. miles were not scored using Climatch because they are already present
in the RA area (i.e., the climate is already known to be suitable). Additionally, D. bellus
and P. heterura were not scored due to incomplete data on native distribution. Of the
ten species that were scored, eight received a high climate match, two received a
medium climate match, and zero species received a low climate match (Table 4-1). The
CCA increased the relative risk score of seven species, resulted in no change in the
relative risk score of four species, and a decreased the relative risk score of three
species (Table 4-1). Three species, D. brachypterus, D. zebra, and P. antennata,
received a climate 6 proportion of 1.0. Climate match did not have a significant influence
on mean BRA (F1,9 = 1.01, r2 = 0.11, p = 0.343).
Maximum body size ranged from a minimum of 13.0 cm total length (TL) for D.
biocellatus to 45.0 cm for P. volitans and P. miles (Table 4-1), with an average
maximum body size of 30.0 cm (SD = 10.64) for Pterois and 17.3 (SD = 4.58) for
70
Dendrochirus. Maximum body size had a significant positive relationship with mean
BRA (F1,13 = 10.87, r2 = 0.48, p = 0.006).
Assessment Review
Overall, changes resulting from the review process were minor and did not result
in major changes to mean scores. The reviewer identified differing degrees of
confidence in the quality of climate matching data (Q5), differing interpretations of non-
aquarium release pathways (Q7), differing interpretations of habitat data relative to
variation in the water velocity of those habitats (Q23), differing interpretations of what
constitutes success at low population density (Q25), and differing interpretations of the
influence of climate change relative to species establishment (Q51).
The reviewer identified D. barberi, D. zebra, P. radiata, and P. russelii as species
with a high BRA delta or CCA delta that warranted further investigation into the source
of variability. One assessor changed the response to Q4 from a low to a medium
climate match for D. barberi, but the change in response did not result in an increase or
decrease in BRA or CCA. One assessor changed the response to Q17 from no to yes
regarding the climatic adaptability of P. radiata, resulting in an increase in the BRA and
CCA score from a 5 to a 7, which increased the mean BRA from a score of 8 to 8.7, and
the mean CCA from a score of 8.7 to 9.3. One assessor changed the response to Q20
regarding the potential to serve as a vector for infectious agents endemic to the RA area
from yes to no for P. lunulata, P. miles, P. russelii, and P. volitans, which resulted in a
decreased BRA and CCA score of one point, and a decreased mean BRA and CCA
score of 0.3.
71
Discussion
Despite overall similarities in morphology, lionfishes exhibited a range of risk
scores. I report relatively low risk scores for lionfishes that lack invasion history, with a
few notable exceptions. As expected, the invasive complex scored higher than any
other species. The highest scoring species outside the invasive complex was P. russelii,
followed by D. brachypterus and P. lunulata. The assessment identified many
similarities between the invasive complex and its close congeners P. russelii and P.
lunulata. Smaller bodied species tended to score lower than those with larger maximum
body sizes (Table 4-1). This is partly due to the “tankbuster” effect where larger
specimens are more likely to be released into the environment (Holmberg et al. 2015)
and because lionfishes are gape limited generalist predators; thus, larger body size may
enable larger prey sizes and a potentially greater effect on native fishes. Climate match
was high for most species but was not a consistent indicator of risk score, despite the
importance of climatic similarity in previous studies (Bomford et al. 2010). This study is
the largest risk screen of marine fishes to date, it identifies a useful research direction
for improving proactive management, and suggests that additional assessment for P.
russelii, D. brachypterus, and P. lunulata may be required.
Invasion history is an important predictor of establishment success (Hayes and
Barry 2008) and a major scoring factor in AS-ISK (Copp et al. 2016), with a maximum
possible obtainable score of 18 for the category “3. Invasive elsewhere”. The total risk
score of both P. volitans and P. miles increased by 65% due to a demonstrated invasion
history, but otherwise scored similarly to P. russelii in their overall biology and ecology.
As such, the risk potential of P. russelii approaches that of the invasive complex.
However, the trade volume of P. russelii is not well documented and the introduction of
72
this species into Atlantic or Gulf waters may be limited by its availability in the marine
ornamental trade (Chapter 3). National import databases report over 30% of lionfishes
imported under the scientific name P. volitans as originating outside of its historical
native range. This suggests that while P. miles and P. russelii are not reported in trade
data, they may be imported in considerable volume under a species misidentification
(Chapter 3). Similarly, P. lunulata scored relatively high, but national import databases
suggest that the trade of this species comprises less than 3% of the total import volume
of lionfishes and this species did not occur in retail surveys (Chapter 3). Discrepancies
in reported trade ultimately affects assessor response and justification to questions
addressing introduction potential and vector strength.
Calibration of AS-ISK and similar taxon-generic tools may prove problematic,
especially for marine fishes. There are currently not enough documented examples of
invasive marine fishes to develop a receiver operating characteristic curve, a method
used to test the predictive ability of the risk assessment tool (Bewick et al. 2004). The
diversity of species for which the tool can be applied is great, and inherent differences in
life histories across taxa can have a considerable impact on scoring and ultimately
calibration. For example, Q37 addresses the ability of taxa to attach to hard substrata, a
characteristic that is not likely to apply to marine fishes, but very likely to apply to a
marine biofouling community. Because of these inherent differences in scoring across
taxa, calibration thresholds that utilize multiple broad taxonomic groups should be
interpreted with caution. Given the importance of climate on non-native species
establishment (Hayes and Barry 2008; Lawson et al. 2013), climatic differences among
RA areas should require that the tool is calibrated on a regional scale. Similarly, human
73
use of fishes in the RA area (e.g. the activity of ornamental collectors), a wide range of
region-specific biological and ecological characteristics, and assessor bias will affect
regional scoring. For example, an evaluation of P. miles in the Mediterranean scored
invasion risk considerably higher than the present study, with the largest scoring
differences from the present study originating from resource exploitation (Q26-27) (Filiz
et al. 2017). However, risk scores of lionfishes can be evaluated using the risk scores of
closely-related known invaders such as P. volitans and P. miles applied to a common
RA area, without the concern of scoring differences across taxa, assessors, or climatic
region.
Risk assessment must cope with inherent uncertainty where data are
lacking (Sikder et al. 2006), which can reduce the predictive ability of risk tools (Orr
2003). The combined research output for all species of lionfishes outside of the invasive
complex is less than 10% of that addressing the invasive complex (Chapter 2), despite
the inclusion of many of these species as research priorities in a national lionfish
prevention and management plan (ANSTF 2014). This is reflected in a higher mean CF
for the invasive complex (0.72) compared to other lionfishes (0.59), and is also reflected
in the low CF of species with severely reduced or lacking bodies of literature (e.g. D.
bellus, Chapter 2). Such a lack of data prevented assessor ability to score several
species of lionfishes that have been recently described (see Methods). The mean CF
across all lionfishes is lower than the mean CF reported for a variety of more intensively
studied freshwater fishes (Glamuzina et al. 2017; Hill et al. 2017; Li et al. 2017).
Targeted research on this group is limited because Pteroinae does not contain any
major sportfishes, is not typically targeted as a food fishery, and is not present in
74
aquaculture. Overall the CF of Pterois is greater than that of Dendrochirus, but when the
invasive complex is removed, mean CF is equal (0.60). This highlights a trend in
research where effort is placed on species after they have become abundant in an
invaded range (Crooks 2005). Previous reviews of the lionfish literature reinforce this
trend, where the bulk of literature addressing the invasive complex was published in the
last decade following spread (Côté and Smith 2018, Chapter 2). Future research should
seek to address some of the data gaps associated with higher-risk lionfishes, namely P.
russelii, D. brachypterus, and P. lunulata.
While recent efforts have been made to clarify the taxonomy of the
Pteroinae (Matsunuma et al. 2017; Wilcox et al. 2018), many species have only a single
publication addressing this important issue (Chapter 2). The polyphyletic genera Pterois
and Dendrochirus may be subjected to discrepancies in assessor definitions of invasive
congeners (Q3), depending on whether they adhere to current systematics or consider
literature that suggests systematic revision (Kochzius et al. 2003; Freshwater et al.
2009). Species that have historically been considered widespread have been
separated, resulting in the biological and ecological characteristics of multiple species
collated into one dataset (e.g. Matsunuma and Motomura 2016). The taxonomy of the
large-bodied Pterois may not be valid, given recent evidence of over-splitting and
hybridization (Wilcox et al. 2018).
Once a non-native species establishes and spreads, eradication becomes costly
and often unfeasible (Molnar et al. 2008), particularly in environments without distinct
boundaries (N’Guyen et al. 2017). Persistence traits and rapid growth characteristics of
the invasive complex make control especially difficult and the results of control overall
75
have been negligible (Dahl et al. 2016), although some positive effects have been
observed on local scales (Frazer et al. 2012). Identifying risk-prone species or groups of
species prior to introduction addresses the first step of the invasion pathway, which can
provide economic savings compared to population control (Leung et al. 2002; Jenkins
2013). Other management options target the establishment or spread of non-native
species, two downstream processes that only occur post-introduction. While such
management responses can be useful for eradicating incipient populations (Simberloff
2003; Vander Zanden et al. 2010) or mitigating the impacts of broadly distributed
populations (e.g. Wagner et al. 2006; N’Guyen et al. 2017), they are not considered
alternatives to prevention.
Ultimately, this rapid risk screen identifies a low invasion risk for most species of
lionfishes. Future risk assessment prioritization should consider the importance of a
group’s invasion history in predicting establishment success (Hayes and Barry 2008),
particularly for marine fishes where risk assessment is uncommon. State and federal
management agencies within the western Atlantic, Gulf of Mexico, and Caribbean
should consider a more in-depth evaluation of the three species with elevated risk, P.
russelii, D. brachypterus, and P. lunulata, which can ultimately be used as an informed
basis for future management action. In addition to proactive risk assessment, regular
action should be taken to maintain and improve early detection and rapid response
networks to provide the most comprehensive and cost-effective risk mitigation
framework (Vander Zanden et al. 2010).
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Table 4-2. Aquatic Species Invasiveness Screening Kit results applied to the State of Florida for 14 species of lionfishes in the genera Pterois, Dendrochirus, and Parapterois.
Species Mean BRA Delta BRA Mean CCA Delta CCA Mean CF Max size TL (cm) Climate 6
Pterois volitans 34.0 2 (33-35) 36.7 5 (34-39) 0.74 45.0 *
Pterois miles 34.0 3 (32-35) 36.7 4 (35-39) 0.70 45.0 *
Pterois russelii 17.7 10 (12-22) 20.3 6 (18-24) 0.59 30.0 0.79
Dendrochirus brachypterus 11.7 5 (9-14) 11.7 5 (9-14) 0.65 17.0 1.00
Pterois lunulata 10.7 3 (9-12) 10.0 5 (7-12) 0.60 35.0 0.49
Pterois radiata 8.7 5 (7-12) 9.3 7 (7-14) 0.61 24.0 0.96
Pterois antennata 8.3 2 (7-9) 8.3 2 (7-9) 0.61 20.0 1.00
Dendrochirus zebra 7.3 6 (4-10) 8.0 4 (6-10) 0.63 25.0 1.00
Pterois mombasae 7.3 1 (7-8) 8.7 3 (7-10) 0.57 20.0 0.82
Pterois sphex 6.3 3 (5-8) 6.3 3 (5-8) 0.59 21.0 0.02
Dendrochirus barberi 3.0 5 (2-6) 1.7 10 (-4-6) 0.60 16.5 0.02
Dendrochirus biocellatus 3.0 2 (2-4) 3.0 2 (2-4) 0.59 13.0 0.88
Parapterois heterura 2.7 4 (0-4) -0.7 4 (-2-2) 0.52 38.0 *
Dendrochirus bellus -0.3 2 (-1-1) 0.3 2 (-1-1) 0.51 15.0 *
Species are arranged from highest to lowest mean BRA score. Multiple assessor scores (n = 3 per species) resulted in a mean BRA (Basic Risk Assessment), delta BRA (min-max), mean CCA (Climate Change Assessment), delta CCA (min-max), and a mean CF (Confidence Factor). Also included are the maximum recorded sizes of each species, and a climate 6 proportion used to estimate climate suitability. * indicates species that are already present in the RA area, or those that do not have enough information on historical range to perform a climate matching model.
77
Figure 4-1. Mean (±SD) basic risk assessment and climate change assessment AS-ISK scores for 14 species of ornamental lionfishes.
78
Figure 4-2. Mean (±SD) score partitioning for nine Aquatic Species Invasiveness
Screening Kit (AS-ISK) scoring categories used to evaluate the risk of the invasive lionfish complex (A) and the risk of 12 additional species of lionfishes found in the ornamental pathway (B). Questions are assigned to nine categories. The overall BRA score is the sum of scores for the top eight categories, and the CCA is the sum of scores for all nine categories. Categories and corresponding question numbers are domestication/ cultivation (Q1-3), climate and distribution (Q4-8), invasive elsewhere (Q9-13), undesirable traits (Q14-25), resource exploitation (Q26-27), reproduction (Q28-34), dispersal mechanisms (Q35-43), tolerance attributes (Q44-49), and climate change (Q50-55).
79
CHAPTER 5 CONCLUSION
The global trade in marine ornamental fishes includes a broad diversity of
species in trade (Rhyne et al. 2012), and is a documented source of non-native species
introductions (Semmens et al. 2004; Schofield et al. 2009). Few species associated with
this pathway have established and spread (Schofield et al. 2009), with the exception of
the lionfish complex that has had widespread impacts in the western Atlantic. The
invasive lionfish complex P. volitans and P. miles was first documented in South Florida
in 1985, and has since established and spread throughout the southeastern US, Gulf of
Mexico, and Greater Caribbean (Schofield 2010). Despite documented evidence of
invader impacts on the species diversity, species abundance, and recruitment success
of native fishes (Albins and Hixon 2008; Albins 2013, 2015), little effort has been made
to address a number of other lionfishes in the ornamental pathway that may present a
similar invasion risk. This thesis examined the literature addressing the other lionfishes
in the genera Pterois, Dendrochirus, and Parapterois, their diversity and volume in the
US ornamental trade, and their potential invasion risk in the State of Florida.
Proactive management is difficult to apply to the marine ornamental trade given
its diversity and scale, especially considering the amount of time and effort required to
assess the of risk for a large pool of potential invaders (e.g., Horizon Scanning, Roy et
al. 2014). Because such a task is often impractical, it is useful to focus proactive
management efforts on groups of fishes most likely to pose invasion risk. There are
many criteria that may be applied across taxa to identify invasion risk, but high
propagule pressure and previous invasion history in a closely related species or group
of species are two widely accepted and strongly influential predictors of invasion
80
success (Hayes and Barry 2008; Lockwood et al. 2009). Therefore, the subfamily
Pteroinae is an ideal group for assessment because it meets the criteria of a
documented pathway (Chapter 3), and shares common characteristics with the invasive
lionfish complex.
Proactive risk management often includes a high level of uncertainty, the majority
of which can be attributed to the lack of data (Orr 2003). This is especially true for
groups of fishes that are not fished for sport, commercially harvested, or produced in an
aquaculture setting (Chapter 2). It is important for risk assessors and managers to
understand how the underlying trends of uncertainty change temporally across the
invasion process and how such limitations affect the predictive accuracy of proactive
risk assessment. In chapter 2, I explored the dynamics of uncertainty within proactive
management by using the lionfishes as a case study. I found that lionfishes without
invasion history are data poor, especially when compared to the already established
invasive complex (Chapter 2). Additionally, I demonstrated the utility of using alternative
sources of information to supplement proactive risk assessment for data poor species
by comparing the primary literature to a report generated during a risk screen of the
Pteroinae in the State of Florida, with the caveat that those sources may be of reduced
quality. Ultimately, the collation of alternative data sources aids in filling data gaps
during the risk assessment phase, and continuing to use such sources of information is
recommended. Some have stressed that a basic understanding of an introduced
species is not required for effective rapid response (Simberloff 2003). I suggest that
preliminary data collection and rapid response can be deployed in tandem to better
81
inform risk management and control if eradication fails, or in the event of future
introductions, particularly in expansive systems.
Propagule pressure has a direct influence on the probability that a non-native
species will overcome environmental and genetic stochasticity to successfully establish
outside the native range (Shaffer 1987; Lande 1988; Hayes and Barry 2008; Lockwood
et al. 2009; Simberloff 2009; Briski et al. 2012). However, propagule pressure is difficult
to measure directly because early-stage invasion data are often absent (Lockwood et al.
2009). As such, research that addresses propagule pressure often uses surrogate
measures, including anthropogenic movement during shipping, trade (Colautti et al.
2009), and leisure activities (McKinney 2002), and the movement of species for human
use (Semmens et al. 2004). In chapter 3, I characterize the trade of lionfishes in the US
using the U.S. Fish and Wildlife Services national import database (LEMIS), as well as
two state databases to capture domestic the movement of lionfishes (Florida and
Hawaii). In addition, I evaluate the diversity and volume of lionfishes in 10 coastal states
at the retail level using standardized surveys. The marine ornamental trade provides a
strong pathway for two species of lionfishes, and a moderate to weak pathway for
others (Chapter 3). The distribution of lionfishes imported into the US is heavily
concentrated at the port of Los Angeles. Retail surveys indicate the lionfish diversity
available directly to hobbyists is reduced when compared to the diversity of imported
species and the diversity of lionfishes advertised to the public through online sales,
suggesting that some species of lionfishes may incur substantial mortality throughout
the pathway due to shipping and consolidation stresses. The risk of introduction for
marine ornamental fishes is concentrated at the end of the trade pathway (i.e. the
82
hobbyist level) (Zajicek et al. 2009), and therefore it is crucial to identify the volume and
diversity of species at the retail level. Ultimately, these data are highly applicable to
proactive risk management in identifying the spatial distribution of introduction risk.
Such characterizations can be used procedurally to further focus risk assessment
towards species that are available to hobbyists in high volume.
Rapid risk screening is a useful and practical first step within a proactive risk
management framework because it can be applied to relatively data poor species in a
time-efficient manner, and can inform more comprehensive risk assessment (Copp et
al. 2016). In chapter 4, I applied the Aquatic Species Invasiveness Screening Kit (Copp
et al. 2016), a questionnaire style semi-quantitative risk screening tool, to 14 species of
lionfishes in the genera Pterois, Dendrochirus, and Parapterois to evaluate their
invasion risk in the coastal waters of Florida and compared them to risk scores
generated for the invasive complex. The invasion risk of the Pteroinae was low to
moderate for most species, with an elevated risk score for P. russelii, D. brachypterus,
and D. lunulata. I recommend the further evaluation of these species for state and
federal managers in the western Atlantic, Gulf of Mexico, and Caribbean. Future risk
assessment should weigh the importance of previous invasion history by focusing effort
on groups of fishes that share similar characteristics with known invaders. This study is
the largest risk assessment of marine ornamental fishes to date, and demonstrates the
utility of rapid risk screening in identifying potentially risky fishes that warrant further
research and possible management action.
Ultimately, rapid risk screening tools benefit from being coupled with 1) the
identification of deficiencies in data inputs that feed into rapid risk screening so that
83
future research effort can be taken to fill crucial gaps, 2) a characterization of
introduction pathways so that potential spatial and species variation can be accounted
for and weighed accordingly, and 3) a targeted approach to risk assessment determined
by demonstrated predictors of invasion success (e.g. high propagule pressure and
shared invasion history). These components provide a holistic approach to rapid risk
screening that serves as a useful first step in identifying potential invaders.
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APPENDIX AQUATIC SPECIES INVASIVENESS SCREENING KIT QUESTION SCHEME
Table A-1. Aquatic Species Invasiveness Screening Kit question scheme.
Question Code Query A. Biogeography/Historical
1. Domestication/Cultivation
1 1.01 Has the taxon been the subject of domestication (or cultivation) for at least 20 generations?
2 1.02 Is the taxon harvested in the wild and likely to be sold or used in its live form?
3 1.03 Does the taxon have invasive races, varieties, sub-taxa or congeners?
2. Climate, distribution and introduction risk
4 2.01 How similar are the climatic conditions of the RA area and the taxon's native range?
5 2.02 What is the quality of the climate matching data?
6 2.03 Is the taxon already present outside of captivity in the RA area?
7 2.04 How many potential vectors could the taxon use to enter in the RA area?
8 2.05 Is the taxon currently found in close proximity to, and likely to enter into, the RA area in the near future (e.g. unintentional and intentional introductions)?
3. Invasive elsewhere
9 3.01 Has the taxon become naturalised (established viable populations) outside its native range?
10 3.02 In the taxon's introduced range, are there known adverse impacts to wild stocks or commercial taxa?
11 3.03 In the taxon's introduced range, are there known adverse impacts to aquaculture?
12 3.04 In the taxon's introduced range, are there known adverse impacts to ecosystem services?
13 3.05 In the taxon's introduced range, are there known adverse socio-economic impacts?
B. Biology/Ecology
4. Undesirable (or persistence) traits
14 4.01 Is it likely that the taxon will be poisonous or pose other risks to human health?
15 4.02 Is it likely that the taxon will smother one or more native taxa (that are not threatened or protected)?
16 4.03 Are there threatened or protected taxa that the non-native taxon would parasitise in the RA area?
17 4.04 Is the taxon adaptable in terms of climatic and other environmental conditions, thus enhancing its potential persistence if it has invaded or could invade the RA area?
18 4.05 Is the taxon likely to disrupt food-web structure/function in aquatic ecosystems it has or is likely to invade in the RA area?
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Table A-1. Continued
Question Code Query
19 4.06 Is the taxon likely to exert adverse impacts on ecosystem services in the RA area?
20 4.07 Is it likely that the taxon will host, and/or act as a vector for, recognised pests and infectious agents that are endemic in the RA area?
21 4.08 Is it likely that the taxon will host, and/or act as a vector for, recognised pests and infectious agents that are absent from (novel to) the RA area?
22 4.09 Is it likely that the taxon will achieve a body size that will make it more likely to be released from captivity?
23 4.1 Is the taxon capable of sustaining itself in a range of water velocity conditions (e.g. versatile in habitat use)?
24 4.11 Is it likely that the taxon's mode of existence (e.g. excretion of by-products) or behaviours (e.g. feeding) will reduce habitat quality for native taxa?
25 4.12 Is the taxon likely to maintain a viable population even when present in low densities (or persisting in adverse conditions by way of a dormant form)?
5. Resource exploitation
26 5.01 Is the taxon likely to consume threatened or protected native taxa in RA area?
27 5.02 Is the taxon likely to sequester food resources (including nutrients) to the detriment of native taxa in the RA area?
6. Reproduction
28 6.01 Is the taxon likely to exhibit parental care and/or to reduce age-at-maturity in response to environmental conditions?
29 6.02 Is the taxon likely to produce viable gametes or propagules (in the RA area)?
30 6.03 Is the taxon likely to hybridize naturally with native taxa?
31 6.04 Is the taxon likely to be hermaphroditic or to display asexual reproduction?
32 6.05 Is the taxon dependent on the presence of another taxon (or specific habitat features) to complete its life cycle?
33 6.06 Is the taxon known (or likely) to produce a large number of propagules or offspring within a short time span (e.g. <1 year)?
34 6.07 How many time units (days, months, years) does the taxon require to reach the age-at-first-reproduction? [In the Justification field, indicate the relevant time unit being used.]
7. Dispersal mechanisms
35 7.01 How many potential internal pathways could the taxon use to disperse within the RA area (with suitable habitats nearby)?
36 7.02 Will any of these pathways bring the taxon in close proximity to one or more protected areas (e.g. MCZ, MPA, SSSI)?
37 7.03 Does the taxon have a means of actively attaching itself to hard substrata (e.g. ship hulls, pilings, buoys) such that it enhances the likelihood of dispersal?
86
Table A-1. Continued Question Code Query
38 7.04 Is natural dispersal of the taxon likely to occur as eggs (for animals) or as propagules (for plants: seeds, spores) in the RA area?
39 7.05 Is natural dispersal of the taxon likely to occur as larvae/juveniles (for animals) or as fragments/seedlings (for plants) in the RA area?
40 7.06 Are older life stages of the taxon likely to migrate in the RA area for reproduction?
41 7.07 Are propagules or eggs of the taxon likely to be dispersed in the RA area by other animals?
42 7.08 Is dispersal of the taxon along any of the pathways mentioned in the previous seven questions (7.01–7.07; i.e. both unintentional or intentional) likely to be rapid?
43 7.09 Is dispersal of the taxon density dependent? 8. Tolerance attributes
44 8.01 Is the taxon able to withstand being out of water for extended periods (e.g. minimum of one or more hours) at some stage of its life cycle?
45 8.02 Is the taxon tolerant of a wide range of water quality conditions relevant to that taxon? [In the Justification field, indicate the relevant water quality variable(s) being considered.]
46 8.03 Can the taxon be controlled or eradicated in the wild with chemical, biological, or other agents/means?
47 8.04 Is the taxon likely to tolerate or benefit from environmental/human disturbance?
48 8.05 Is the taxon able to tolerate salinity levels that are higher or lower than those found in its usual environment?
49 8.06 Are there effective natural enemies (predators) of the taxon present in the RA area?
C. Climate change
9. Climate change
50 9.01 Under the predicted future climatic conditions, are the risks of entry into the RA area posed by the taxon likely to increase, decrease or not change?
51 9.02 Under the predicted future climatic conditions, are the risks of establishment posed by the taxon likely to increase, decrease or not change?
52 9.03 Under the predicted future climatic conditions, are the risks of dispersal within the RA area posed by the taxon likely to increase, decrease or not change?
53 9.04 Under the predicted future climatic conditions, what is the likely magnitude of future potential impacts on biodiversity and/or ecological integrity/status?
54 9.05 Under the predicted future climatic conditions, what is the likely magnitude of future potential impacts on ecosystem structure and/or function?
55 9.06 Under the predicted future climatic conditions, what is the likely magnitude of future potential impacts on ecosystem services/socio-economic factors?
87
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BIOGRAPHICAL SKETCH
Tim was born in Miami, Florida where he grew up and attended school at Miami
Palmetto Senior High. His younger years were spent diving and maintaining reef
aquariums, where he grew to appreciate Florida’s coastal ecosystems. Upon graduating
primary school, he turned his fondness for marine life into a career by enrolling in the
Univeristy of Florida’s school of Fisheries and Aquatic Sciences in August of 2013.
While pursuing his Bachelor of Science degree with a concentration in marine
science, he further strengthened his career choice and professional skills through
coursework and extracurricular activity. In May 2015, he took a position as a research
intern in Apollo Beach, where he further improved his marine aquaculture experience.
He graduated with his Bachelor of Science from the University of Florida in April of
2016.
Shortly after graduation, Tim accepted a position as a research intern at the
Univeristy of Florida’s Tropical Aquaculture Laboratory in Ruskin, Florida. Here, he
began working towards a Master of Science degree in fisheries and aquatic sciences.
During his time as a graduate student, he shifted his focus to invasion ecology and
applied his research towards the proactive risk management of lionfishes. Following
completion of his graduate degree, Tim accepted a position with the Albuquerque
Biological Park as an IUCN Red List Officer with a focus on aquatic species.
