The Role of Biotic and Environmental Factors in Spatial and Temporal Variability of Indian River Lagoon Copepod Communities

by Hannah G. Kolb

B.S. Oceanography Florida Institute of Technology 2011

A thesis submitted to Florida Institute of Technology in partial fulfillment of the requirements for the degree of

Master of Science in Biological Oceanography

Department of Ocean Engineering and Sciences

Melbourne, Florida

December 2016

The Role of Biotic and Environmental Factors in Spatial and Temporal Variability of Indian River Lagoon Copepod Communities A Thesis by Hannah G. Kolb

Approved as to style and content by:

______Kevin B. Johnson, Ph.D. Associate Professor, Oceanography

______John Windsor, Ph.D. Professor Emeritus, Oceanography

______Jonathan Shenker, Ph.D. Associate Professor, Biological Sciences

______Stephen Wood, Ph.D. Department Head, DOES

December 2016

ABSTRACT

The Role of Biotic and Environmental Factors in Spatial and Temporal Variability of Indian River Lagoon Copepod Communities

by Hannah G. Kolb B.S. Oceanography, Florida Institute of Technology Department of Ocean Engineering and Sciences Major Academic Advisor: Kevin B. Johnson, Ph.D.

The role of zooplankton communities as the link between phytoplankton and secondary consumers is dependent on the species make-up of the copepod community. Copepods often dominate zooplankton in numbers and biomass and are frequently the dominant grazers. Species variabilities in behavioral and morphological traits, and seasonal variances in species make-up, have the potential to alter trophic dynamics in planktonic communities. The goal of this study was to identify the driving forces behind copepod community composition and better understand the role of key species in the Northern Indian River Lagoon

(N-IRL). Copepods made up 76% of the N-IRL zooplankton community and have average densities of 2.3•104 ± 4.5•103 m-3. Three dominant species, Acartia tonsa,

Oithona colcarva, and Parvocalanus crassirostris, make up >95% of the total copepod abundances. The relative dominance of these species shifts spatially

iii

between sites (p<0.01) and temporally between wet and dry seasons (p<0.05).

Likely intrazooplanktonic predators (the chaetognath Sagitta sp., the ctenophore

Mnemiopsis leidyi, and larval fish) had no apparent impact on copepod community abundance. Of all abiotic and biotic factors examined, copepod composition was most closely correlated to relative chlorophyll and Secchi depth (R=0.41), both of which were impacted by algal bloom events. Although communities did not display strong seasonality, their densities and composition do seem to be driven from the bottom up.

ACKNOWLEDGEMENTS

This project would never have been completed without the support of so many people. I first want to thank my advisor Dr. Kevin Johnson for encouraging me down the zooplankton path and for his patience and guidance though the dozens of drafts. Thank you, Dr. John Windsor, for asking hard questions and not always expecting an answer. Thank you, Dr. Jon Shenker, for contributing your expertise to produce this finished product. Thank you, Holly Sweat, for being my field and laboratory partner over the past 3 years and for patiently answering my never- ending questions. Thank you, Bill Battin, for being a friendly face on the bad days and always helping me get the job done. Thank you, Xiao Ma, Angel Seery, Tony

Cox, Casey Hederman, and Kate Beckett, for being so willing to spend long days on the water so I could get my samples. Thank you, Xiao Ma and Angel Seery, for your help in the lab with the most boring of tasks. Thank you, Casey Hederman, for making the unreadable readable. Thank you to my sisters Sarah and Rachel for always encouraging me. Most of all, thank you to my parents Roger and Mary Kay

Kolb for encouraging my love of nature from the start and for always supporting me in whatever I do.

Table of Contents

ABSTRACT ...... iii

ACKNOWLEDGEMENTS ...... v

LIST OF TABLES AND FIGURES ...... viii Tables ...... viii

Figures ...... x

INTRODUCTION ...... 1 Community Succession ...... 2

Regulation of Planktonic Populations ...... 3

Bottom-up Controls ...... 5

Location...... 5

METHODS ...... 6 Study Site Description ...... 6

Field Methods ...... 8

Laboratory Processing ...... 9

Analysis ...... 9

RESULTS ...... 10 Community Make-up ...... 10

Wet/Dry Season Variability in the Copepod Community ...... 18

Environmental Factors ...... 19

Impact of Algal Blooms on Community Composition ...... 26

Intraplanktonic Predators ...... 28

DISCUSSION ...... 33 Dominant Species ...... 33

Biotic Factors ...... 35

Seasonal Patterns in Copepod Communities ...... 35

Potential Predation Effects ...... 36

Environmental Factors ...... 41

Biotic Versus Abiotic Factors ...... 42

Copepod Community Function ...... 42

CONCLUSIONS ...... 44

REFERENCES ...... 46

APPENDIX: ...... 54 Average Densities of Dominant Copepod Species by Season and Year ...... 54

vii

LIST OF TABLES AND FIGURES

Tables

(June-Aug), Autumn (Sept-Nov), Winter (Dec-Feb), Spring (Mar-May).

ML=Mosquito Lagoon, TV=Titusville, CV=Cocoa ...... 13

Table 2. Rankings of abundant copepod species that make up >1% of the copepod community. Average % and mean densities (# m-3) represent biweekly replicated samplings (n=4 reps/site) collected June 2013-June 2016. Species contributing <1% to overall composition were excluded...... 15

Table 3. ANOSIM and SIMPER analysis of species contributions per wet/dry season. Samples collected biweekly (n=4 reps/site) June 2013-June 2016.)...... 18

Table 4. Regression analysis of dominant copepod species of the N-IRL with environmental variables. Replicated samplings (n=4 reps/site) were conducted biweekly June 2013-June 2016 ...... 23

Table 5. ANOSIM/SIMPER analysis of species percent contributions under bloom and non-bloom conditions. Densities (# m-3) fourth-root transformed to reduce weight of abundant species. Samples collected June 2013-June 2016...... 27

viii

Figures

Figure 1. Locations of sampling sites within the Northern Indian River Lagoon, FL

(modified from Google Maps image)...... 7

Figure 2. Mean densities ± SE of dominant copepod species of the N-IRL from June

2013 to June 2016. Densities (# m-3) represent seasonal averages of biweekly replicated samplings (n=4 reps/site)...... 12

Figure 3. Dominant copepod species of the Northern Indian River Lagoon a)

Acartia tonsa b) Oithona colcarva c) Parvocalanus crassirostris. Photos by L. H.

Sweat...... 14

Figure 4. a) Historical algal taxa abundances (# 1000m-3) (Badylak and Phlips, 2004) and b) observed copepod mean densities (# m-3) June 2013-June 2016 at sites in the Northern Indian River Lagoon, FL...... 17

Figure 5. Seasonal variation in species make-up (%) of the copepod community.

Samples collected biweekly June 2013-June 2016...... 19

Figure 6. Environmental conditions of surface waters at sites a) temperature (°C) b) salinity (ppt) c) relative chlorophyll (µg L-1) d) Secchi depth (cm). Temperature, salinity, and Secchi depth were collected in field at time of sampling, relative chlorophyll was gathered from the closest SJRWMD continuous sensor-based water quality monitoring station (SJRWMD, 2016)...... 22

Figure 7. a) Wet and Dry season salinities (ppt) from June 2013-June 2016 compared to b) the deviation of seasonal rainfall totals from historical averages

(in) (SJRWMD, 2016)...... 24

Figure 8. Densities of dominant copepod species relative to salinity (ppt). Samples collected biweekly (n=4 reps/site) June 2013-June 2016. A. tonsa (p=0.03, R2=0.03, slope=-413), O. colcarva (p<0.001, R2=0.15, slope=-516), P. crassirostris (p<0.001,

R2=0.12, slope=-615). Slopes were significantly different between species of copepods (p=1.37•10-5)...... 25

Figure 9. Copepod community density (# m-3) under bloom and non-bloom conditions. Samples collected biweekly June 2013-June 2016 (n=4 reps/site)...... 27

Figure 10. Life stages of juvenile (<1.5cm) and adult (> 1.5cm) Mnemiopsis leidyi.

Samples collected biweekly (n=4 reps/site) from Sept. 2013-June 2016. Mean densities (# m-3) represent organisms > 0.5cm. Life stage classifications based on field measurements of organism length and samples were not retained...... 30

Figure 11. Mean densities (# m-3) of copepod predators, Sagitta sp. and fish larvae collected biweekly (n=4 reps/site) June 2013-June 2016...... 31

Figure 12. Mnemiopsis leidyi feedback cycle resulting from stage-dependent behavior (adapted from McNamara et al., 2013) ...... 39

INTRODUCTION

In aquatic food webs, zooplankton act as the link between primary producers and consumers. Copepods often dominate the zooplankton in numbers and biomass and are considered important grazers (Field, 1892; With and Hansen, 1915;

Sommer and Sommer, 2006; Sommer and Stibor, 2002). Many food web studies describe a simple linear trophic transfer of nutrients→phytoplankton→zooplankton→fish (Sommer and Stibor, 2002).

However, because of the large variability of behavioral and morphological traits within the copepod class, a change in the species make-up can alter the role of the copepod community in a food web (Dakin, 1908; Kleppel, 1993; Sprules and

Bowerman, 1988; Winder and Jassby, 2011). Seasonal shifts in dominant species may thus alter planktonic food webs. Variability in the physiology, diet, feeding mechanisms, development, and environmental ranges of different copepod species will result in commensurate changes to copepod impacts on the ecosystem. This study examines the environmental factors and food web dynamics that affect copepod community make-up in the Northern Indian River

Lagoon (N-IRL), including a characterization of the dominant copepod species. I also examine the role environmental factors and predators play in shaping the copepod community.

Community Succession

In 1961, G.E. Hutchinson wrote “The paradox of the plankton,” in which he discussed the seemingly paradoxical situation of phytoplankton diversity. He observed that plankton communities are as functionally diverse, and show the same richness of interaction, as terrestrial communities, but occur in an apparently “niche”-poor ecosystem. According to the principle of competitive exclusion (Gause, 1936), the number of organisms that can co-exist in a system equals the number of niches in that system. The one best-adapted species for a niche will emerge as dominant and drive the others towards extinction. He theorized that co-existence of multiple prey species is made possible when competing species face different predators or differential selection by a predator

(i.e., predation subtleties are part of the niche). This theory set the foundation for planktonic community succession (Gliwicz and Pijanowska, 1989; Sommer et al.,

1986; and Sommer et al., 2012).

Succession is defined as a predictable, directional process of community development through its modification of the physical environment, progressing towards a stabilized ecosystem (Odum, 1969). Succession is a result of biotic interactions, with the potential for interspecific effects in the community. The pattern, rate, and limits of the biotic interactions that lead to succession are determined by the physical environment (Odum, 1969). Biotic interactions in the

plankton include grazing, predation, and competition. These three interactions are dependent on spatial and temporal variability in the interacting species. Countless connections within spatially diverse and temporally dynamic planktonic communities create a complex, ever-changing food web.

The stability of a system refers to its predictability or resistance to change (Paine,

1969). A stable ecosystem may display pronounced temporal fluctuations in abundance and composition, but then must be cyclic, following a predictable order of succession and abundances. Phytoplankton and ichthyoplankton of the N-

IRL both follow predictable cyclic patterns (Badylak and Phlips, 2004; Reyier and

Shenker, 2007). One goal of this study is to determine if the zooplankton that form the link between these trophic levels follow a similar temporal pattern. Copepods are the most abundant grazers in the N-IRL mesozooplankton community

(organisms >200µm) and are a common food for ichthyoplankton and juvenile fish

(Kerr, 2009; Rey et al., 1991). The role of copepods as a link between primary producers and higher trophic levels makes them critical to the overall functioning of the estuarine ecosystem and fisheries.

Regulation of Planktonic Populations

Population size is determined by reproductive output less mortality (Arditi and

Ginzburg, 1989). Reproductive potentials are maximized when the animals thrive under optimal environmental conditions and food availability (Sibly and Hone,

2002). Mortality varies seasonally with the density and type of predators and food

(Sibly and Hone, 2002).

Planktonic community regulation can be driven from the bottom-up, the top- down, or a combination of both. In top-down control, grazers and predators shape the community through their feeding (Estes and Palmisano, 1974; Graneli and Turner, 2002). In bottom-up control, primary production controls the grazer and predator communities through resource limitation (Frederiksen et al., 2006;

Hoover et al., 2006). These means of shaping and controlling a community can be indirect through a competitor or an alternative food source (Estes and Palmisano,

1974; Graneli and Turner, 2002), or direct (Sommer and Sommer, 2006; Frank et al., 2005).

Bottom-up control assumes a positive correlation between the biomasses of different trophic levels, as more prey can support more consumers. Top-down control, on the other hand, assumes negative correlations as more consumers leave less prey.

In the past there was disagreement amongst ecologists on trophic control of community composition (Sommer et al., 2002). Today most acknowledge that both top-down and bottom-up factors have important effects on communities and a combination most likely best describes population and community dynamics.

The question ecologists are asking now is, “how do bottom-up and top-down effects interact?” (Menge, 1992).

Bottom-up Controls

Planktonic grazers may compete for phytoplankton (DeMott, 1989). All things being equal, a fast-growing inefficient grazer species will peak first and then be replaced by slower growing, but more-efficient, species (Huston, 1979). Food preferences and selectivity can increase the opportunity for co-occurrence and may shape succession (Maly and Maly, 1974). Food size specialization by grazing species can decrease competition pressure (Wilson, 1975). Larger species feeding on all size particles may gain a competitive advantage over size-restricted grazers

(Brooks and Dodson, 1965). On the other hand, selective grazers may focus on higher quality food and gain an advantage over nonselective species (DeMott,

1989). The degree of interspecific food competition amongst copepods is also dependent upon their positioning in the water column, including daily vertical migration behaviors (Fulton III, 1984a). Species with identical food requirements, but separated spatially, will not compete. Migrations can therefore reduce competition, or at least limit it to temporary spatial overlaps.

Location

This study examined zooplankton trophic dynamics in Florida’s Indian River

Lagoon (IRL). The IRL is a shallow estuary running 156 miles along Florida’s east

coast. Commercial fisheries within the IRL have been in decline the last 25 years as a result of increased development in the area as well as the recent occurrence of large algal blooms and associated fish kills (NEP, 2009). Shellfish harvests have decreased 72% and fin fish have decreased 54% (ECFRPC, 2016). Establishing a better understanding of the stability and seasonal behaviors of the copepod community should allow for a more complete understanding of the N-IRL system.

This research is aimed at addressing the following hypotheses: 1) Zooplankton communities of the N-IRL are dominantly comprised of characteristic species of copepods; 2) Environmental variables drive copepod community species composition and volume; and 3) Intraplanktonic predators exert top-down control of copepod species composition.

METHODS

Study Site Description

Sampling locations were chosen to represent the main semi-isolated bodies that make up the northern section of the Indian River Lagoon. Three sites were sampled: Mosquito Lagoon near the Haulover Canal, Indian River Lagoon in

Titusville, and Indian River Lagoon in Cocoa (Fig. 1). The Mosquito Lagoon site

(28.731°N, -80.732°W), located within the Merritt Island National Wildlife refuge south of the Haulover canal, is very shallow (<1.5m) and protected. The Titusville site (28.634°N, -80.707°W), located in the Indian River Lagoon south of the

Haulover Canal, is shallow (~1.5m) with little protection. The Cocoa Village site

(28.345°N, -80.716°W), located in the Indian River Lagoon south of the 520

Causeway, is moderately shallow (2-4m) with little protection.

Mosquito Lagoon Titusville

Cocoa

Figure 1. Locations of sampling sites within the Northern Indian River Lagoon, FL (modified from Google Maps image).

Field Methods

Samples analyzed in this study were of daytime surface populations. Sampling occurred biweekly from June 2013 to June 2016. Zooplankton samples were collected using a 153µm mesh net with a mouth diameter of 30cm. The net was towed horizontally within 1 m of the surface, effectively representing the entire water column in these shallow locations. Time length of tows was typically 60 seconds, being shortened when bloom conditions clogged the net. Tow volumes were calculated from tow speeds and confirmed by in-net flowmeters. At each site, on a given sample day, four replicate tows were collected (n=4). Comb jellies, larger organisms, and plant matter were measured and recorded, then removed from the sample. Zooplankton were preserved in 5% formalin, buffered with sodium tetra-borate. Density and size distributions of gelatinous zooplankton were collected. A Secchi disk was used to collect water transparency. The YSI

Castaway CTD was used to collect vertical salinity and temperature profiles of the water column and to determine the degree of stratification. Relative chlorophyll was collected by the St. Johns River Water Management District’s mounted continuous water quality sensors which were located near the Mosquito Lagoon and Titusville sites.

Laboratory Processing

Total settled volumes were collected for each sample, then aliquots were taken using a Motodo plankton splitter. Using a stereomicroscope, zooplankton were classified to the lowest possible taxonomic level. For each sample a minimum of

300 individuals were identified (Davidson and Clem, 2003). Using the measured tow volumes collected for each sample, field densities were calculated.

Analysis

The dominant copepods of the N-IRL were identified by ranking species by density, and proportion of total copepod community. Densities and proportion were compared between sites and between wet and dry season. Diversity analysis in the form of species richness, number of individuals, Shannon index, and Evenness index of the copepod communities was conducted. Site diversity was compared using ANOVA. Seasonal and temporal patterns in overall community composition were examined using ANOSIM and SIMPER analyses (PRIMER v5). Densities (# m-3) were fourth root transformed to reduce the weight of abundant species. To identify possible predator-prey interactions, regression analysis was conducted of

Sagitta sp., Mnemiopsis leidyi, and fish larvae densities versus the densities of dominant copepod species. The degree to which temperature, salinity, relative chlorophyll, and Secchi depth are correlated with the presence and abundance of dominant species, was determined using regression analysis conducted on

dominant species and environmental variables. For variables with significant regressions, slopes were compared across species using ANOVA and T-tests. The relative influences of physical versus biotic factors on copepod communities were compared using Bio-Env analysis (PRIMER v5) with both biotic and physical factors.

The impact of bloom presence on community composition was examined using

ANOSIM and SIMPER (PRIMER v5).

RESULTS

Community Make-up

Copepod species were ranked by density and proportion of total copepod community. Copepods made up 76±1% of mesozooplankton communities by count. Other dominant mesozooplankton groups which made up which contributed to the remaining 24±1% of the mesozooplankton were gastropod veligers (2000±1300 m-3), barnacle nauplii (600±100 m-3), larvaceans (1800±300 m-

3), cladocerans (1700±500 m-3), and chaetognaths (150±30 m-3). None of these groups were as consistently abundant as copepods. Within the N-IRL, regardless of site, the copepod community was primarily (96±0.7%) made up of Acartia tonsa

(Fig. 3a, Table 2), Oithona colcarva (Fig. 3b, Table 2), and Parvocalanus crassirostris (Fig.3c, Table 2). The remaining 4±0.7% of the copepod community was made up of 19 species (Table 1). A. tonsa, O. colcarva, and P. crassirostris were present throughout the study (Table 1). Acartia tonsa was the most

abundant of the species (6300±900 m-3) with Oithona colcarva (3900 ±800 m-3) and Parvocalanus crassirostris (4100 ±1300 m-3) being less abundant (Fig. 2).

Two anomalous events occurred during the study period, a hypersaline event

(>35ppt) from Summer 2013 to Spring and a persisting algal bloom from early

Winter 2015 through Spring 2016 (Fig. 2). During these anomalous events densities and species make-up of the copepod community were altered (Fig. 2).

Mosquito Lagoon a SE

± 10

) )

3 - 8

2 Density (thousand m (thousand Density 0

Titusville SE

± b

) ) 40

3 -

10 Density (thousand m (thousand Density 0

60 Cocoa SE

± c

) ) 3

- 40

0 Density (thousand m (thousand Density

Acartia tonsa Oithona colcarva Parvocalanus crassirostris

Figure 2. Mean densities ± SE of dominant copepod species of the N-IRL from June 2013 to June 2016. Densities (# m-3) represent seasonal averages of biweekly replicated samplings (n=4 reps/site).

Table 1. Seasonal presence/absence patterns of occurrence of all copepod species in N-IRL June 2013 to June 2016. Presence classified as the species being observed in >1 sampling during that seasonal period. Seasons were classified as Summer (June-Aug), Autumn (Sept-Nov), Winter (Dec-Feb), Spring (Mar-May). ML=Mosquito Lagoon, TV=Titusville, CV=Cocoa

NP- no seasonal pattern, ML- Mosquito Lagoon, TV-Titusville, CV-Cocoa Village

a b c

Figure 3. Dominant copepod species of the Northern Indian River Lagoon a) Acartia tonsa b) Oithona colcarva c) Parvocalanus crassirostris. Photos by L. H. Sweat.

Mosquito Lagoon Average % (±SE) Density # m-3 (±SE) Acartia tonsa 51 (±5) 4525 (±490) Oithona colcarva 23 (±4) 2073 (±348) Parvocalanus crassirostris 22 (±5) 1923 (±436) Longipedia sp. 2 (±0.4) 135 (±43) Euterpina acutifrons 3 (±0.5) 227 (±73)

Titusville Average % (±SE) Density # m-3 (±SE) Acartia tonsa 47 (±13) 6742 (±1798) Oithona colcarva 24 (±4) 3375 (±633) Parvocalanus crassirostris 27 (±6) 3891 (±829) Longipedia sp. 1 (±0.3) 118 (±45) Euterpina acutifrons 1 (±0.3) 98 (±38)

Cocoa Average % (±SE) Density # m-3 (±SE) Acartia tonsa 38 (±8) 8166 (±1790) Oithona colcarva 30 (±9) 6437 (±1944) Parvocalanus crassirostris 30 (±12) 6484(±2597) Euterpina acutifrons 1 (±0.6) 190 (±145)

Historically, the standing algal biomass of our sites has been shown to increase from Mosquito Lagoon to Cocoa (Fig. 4a) (Badylack and Phlips, 2004). Similarly, copepod densities increased from Mosquito Lagoon (8000 ±1500 m-3) to Cocoa

(23000 ±5000 m-3) (Fig. 4b). Algal composition at our sites has been shown to be variable, but with characteristic taxa typical in different sub-bodies of the N-IRL

(Fig. 4a) (Badylack and Phlips, 2004). A similar pattern was expected in copepod communities (Fig. 4b). Two-way crossed ANOSIM of copepod communities found significant differences (p<0.01) between community composition of sites. From

North to South the dominance of Acartia tonsa decreased (51, 47, 38%) and the role that Oithona colcarva played in the community increased (23, 24, 30%) (Table

2).

3.5 1 - a

3 m

µ 2.5 Diatoms 2 Dinoflagellates 1.5 Other algae 1

0.5 Mean biovolume million million biovolume Mean 0

25 3 - b 20

15 A. tonsa 10 O. colcarva P. crassirostris

5 Mean densitym thousandMean 0 Mosquito Titusville Cocoa Lagoon

Wet/Dry Season Variability in the Copepod Community

The three most common species A. tonsa, O. colcarva, and P. crassirostris, were present in the copepod community year-round, however their densities and percent contribution varied seasonally (Fig. 2). Two-way crossed ANOSIM of wet versus dry copepod communities found that between wet (May 28-Oct 16) and dry (Oct 17-May 27) season copepod communities varied significantly (p<0.001,

R=0.21). Wet/dry seasons were classified based on the Melbourne NWS classification for wet season in Melbourne, FL (Lascody, 2002). According to

SIMPER analysis difference in community composition is primarily driven by a decreased role of Parvocalanus crassirostris in dry season communities (Table 3 and Fig. 5).

Table 3. ANOSIM and SIMPER analysis of species contributions per wet/dry season. Samples collected biweekly (n=4 reps/site) June 2013-June 2016.).

Wet season Dry season R=0.21, p<0.001 A. tonsa 42% A. tonsa 39%

O. colcarva 28% O. colcarva 31%

P. crassirostris 21% P. crassirostris 11%

2-way ANOVA of wet versus dry season found a significant difference in percent composition between seasons for all species (A. tonsa p<0.005, O. colcarva p<0.05, P. crassirostris p<<0.001).(Fig. 5). There was a significant interaction of year and season with A. tonsa and P. crassirostris.

100 2013/2014 80 60 40

20 Percentage of Percentage

copepod community copepod 0

80 2014/2015 60

Percentage of Percentage copepod community copepod 0

60 2015/2016

20 community 0

Percentage ofcopepod Percentage Acartia tonsa Oithona colcarva Parvocalanus crassirostris Wet Dry

Figure 5. Seasonal variation in species make-up (%) of the copepod community. Samples collected biweekly June 2013-June 2016.

Environmental Factors

Temperatures at all sites followed typical cyclic seasonal patterns (Fig. 6a). For all sites, temperatures remained within the dominant copepod species ranges with

an overall average temperature of 25°C, and minimum temperatures of below

15°C never exceeding more than one sampling (<14days). Parvocalanus crassirostris was the only species to have a correlation to temperature (p<0.01,

R2=0.06, slope=400), with densities only having a weak relationship to changes in temperature.

The Secchi depths at our sites did not exhibit clear seasonal patterns (Fig. 6d).

Secchi depths decreased in late 2015 with the occurrence of phytoplankton blooms. Secchi depths negatively correlated logarithmically with relative chlorophyll (R2=0.13, p<0.001), with transparency of the lagoon declining during bloom events. Oithona colcarva and Parvocalanus crassirostris, species with distinctly different trophic strategies, were positively correlated to Secchi depth.

This correlation was strongest with P. crassirostris, the opportunistic particle feeder.

Relative chlorophyll densities were utilized as a metric of the severity of phytoplankton blooms at the sites. Under typical non-bloom conditions the average relative chlorophyll density was <33µg L-1. During the peak of the phytoplankton bloom relative chlorophyll densities reached >200µg L-1. Multiple bloom densities of algae occurred during the study period and they did not follow a temporal pattern. The largest and longest lasting bloom began building in Sept

2015 and peaked in late Dec 2015. Relative chlorophyll levels remained elevated

through the end of the study period in June 2016. Because of the random temporal pattern of these bloom events, relative chlorophyll levels did not follow a cyclic pattern reflective of wet season nutrient influxes (Fig. 6c).

The 2013 and 2015 sampling years were unusual years for rainfall (Fig. 7a). 2013 had an unusually dry wet season, with rainfall totals 11 inches less than the historical average. 2015 had an unusually wet dry season due to a strong El Niño effect, with totals 9 inches more than the historical average (Fig. 7b). The unusually dry wet season in 2013 coupled with the increasing trend for N-IRL salinities (Mann-Kendall p<0.05, SJRWMD, 2016) resulted in hypersaline conditions at all sites, with Mosquito Lagoon having the highest salinities (Fig. 7a).

All dominant copepod species exhibited a negative correlation to salinity. P. crassirostris and O. colcarva exhibited stronger negative correlations than A. tonsa which is a robust, widely distributed species (Fig. 8).

35 a 30

C) ° ( 20

15 Temperature Temperature 10

55 b 35

Salinity(ppt) 15

500 - c 400

300 )

1 200 Relative Relative 100 Chlorophyll (µg L (µg Chlorophyll 0

400 300 d 200 100

Secchi depth (cm) depth Secchi 0

Jun-13 Jun-14 Jun-15 Jun-16

Sep-13 Sep-14 Sep-15

Dec-13 Dec-14 Dec-15

Mar-14 Mar-15 Mar-16 Mosquito Lagoon Titusville Cocoa Figure 6. Environmental conditions of surface waters at sites a) temperature (°C) b) salinity (ppt) c) relative chlorophyll (µg L-1) d) Secchi depth (cm). Temperature, salinity, and Secchi depth were collected in field at time of sampling, relative chlorophyll was gathered from the closest SJRWMD continuous sensor-based water quality monitoring station (SJRWMD, 2016).

Table 4. Regression analysis of dominant copepod species of the N-IRL with environmental variables. Replicated samplings (n=4 reps/site) were conducted biweekly June 2013-June 2016

Variable Species p- value R2 Slope Temperature Acartia tonsa 0.16 Oithona colcarva 0.42 Parvocalanus crassirostris <0.01 0.06 400 Salinity Acartia tonsa 0.03 0.03 -413 Oithona colcarva <0.001 0.15 -516 Parvocalanus crassirostris <0.001 0.12 -613 Secchi depth Acartia tonsa 0.71 Oithona colcarva 0.02 0.04 19 Parvocalanus crassirostris <0.001 0.13 42 Relative Chlorophyll Acartia tonsa 0.85 Oithona colcarva 0.41 Parvocalanus crassirostris 0.17

a b

Figure 7. a) Wet and Dry season salinities (ppt) from June 2013-June 2016 compared to b) the deviation of seasonal rainfall totals from historical averages (in) (SJRWMD, 2016).

Log (x+1) (x+1) Log transformed 3 - 2

25 1

Density m Density

0 15 20 25 30 35 40 45 Salinity (ppt) Acartia tonsa Oithona colcarva Parvocalanus crassirostris

Results of Bio-Env analysis found a combination of Secchi depth and relative chlorophyll (R=0.41) explained the most variance in copepod community. At all sites, environmental factors had higher correlations than predators with regard to copepod community composition.

Impact of Algal Blooms on Community Composition

Algal bloom events were classified as sampling periods when relative chlorophyll exceeded by 1 standard deviation, the baseline density of a site. Bloom events occurred multiple times throughout the study period for short periods, and a more persistent bloom occurred from early Winter 2015 through the end of the study period (Nov 2015-June 2016). The total copepod community had a significant decrease in density during bloom conditions (p<0.001) (Fig. 9).

Populations also had a significant shift in species make-up (ANOSIM p<0.05,

R=0.08) (Table 5). As relative chlorophyll levels increased during algal blooms, the relative proportion of P. crassirostris decreased from 18% to 5%. The relative contributions of A. tonsa and O. colcarva remained stable (Table 5).

) 3 - 15

Totalcopepod (thousandm

community density 0 Bloom Non-bloom

Figure 9. Copepod community density (# m-3) under bloom and non-bloom conditions. Samples collected biweekly June 2013-June 2016 (n=4 reps/site).

Bloom Non-Bloom R=0.08, p<0.05 A. tonsa 40% A. tonsa 40% O. colcarva 29% O. colcarva 29% P. crassirostris 5% P. crassirostris. 18% E. acutifrons 7% E. acutifrons 6%

Longipedia sp. 10%

Intraplanktonic Predators

The most apparent intraplanktonic predators from June 2013- June 2016 were the chaetognath Sagitta sp. the ctenophore Mnemiopsis leidyi, and a variety of fish larvae. All predator groups exhibited substantial spatial and temporal variability

(Fig. 10 and 11). The southernmost site, Cocoa, had the highest densities of fish larvae, the northernmost site, Mosquito Lagoon, had the highest densities of M. leidyi, and the central site, Titusville, had the highest densities of Sagitta sp. (Fig.

10 and 11).

Mnemiopsis leidyi populations showed seasonal peaks consistent across sites.

Densities peaked during winter months of December to March and in the summer from June to July (Fig. 10). M. leidyi was most abundant and common at the northernmost site, Mosquito Lagoon (Fig. 10a) and least abundant at the southernmost site Cocoa (Fig. 10c). Juvenile M. leidyi (<1cm) occurred more frequently in northern sites and were rarely collected in Cocoa samples (Fig. 10).

Juvenile M. leidyi and O. colcarva, which share a common feeding preference for ciliates, were positively correlated (R2=0.10) (Table 6).

Larval fish populations displayed clear annual cycles, as seen previously (Reyier and Shenker, 2007), peaking in the spring and summer and disappearing during the winter months (Fig. 11). Average larval fish densities were 6.8 ± 1.8 m-3, higher than the densities of 2-6 m-3 previously observed in the area (Reyier and Shenker,

2007). None of the common copepod species displayed strong correlations to larval fish abundance (Table 6).

Sagitta sp. populations exhibited similar patterns of abundance at all sites (Fig.

11). Populations of Sagitta sp. were significantly higher during the summer months (June-Aug) than the winter months (Dec-Feb) (1-way ANOVA, p=0.007).P. crassirostris and O. colcarva exhibited positive correlations with Sagitta sp. (Table

6).

12 a. Mosquito Lagoon 3

- 10

Density Density m 6

M. M. leidyi 2

3 b. Titusville - 4

3 Density Density m 2

1 M. M. leidyi

0.3 3

- c. Cocoa

0.2 Density Density m

0.1 M. M. leidyi

Juvenile Adult

Figure 10. Life stages of juvenile (<1.5cm) and adult (> 1.5cm) Mnemiopsis leidyi. Samples collected biweekly (n=4 reps/site) from Sept. 2013-June 2016. Mean densities (# m-3) represent organisms > 0.5cm. Life stage classifications based on field measurements of organism length and samples were not retained.

2500 a. Mosquito Lagoon 50

Density Fish Larvae m Fish Larvae Density 3

- 2000 40 m

1500 30

Sagitta sp. 1000 20 -

500 10 3 Density Density

0 0

3500 b. Titusville 100 90

3000 m Fish Larvae Density 3 - 80

. . m 2500 70 2000 60 50

Sagittasp 1500 40

1000 30 -

20 3 Density Density 500 10 0 0

3000 200

c. Cocoa 180 m Fish Larvae Density

3 -

2500 160 . . m 2000 140 120 1500 100

Sagittasp 80 1000 60

40 -

500 3 Density Density 20 0 0

Sagitta Fish Larvae

Figure 11. Mean densities (# m-3) of copepod predators, Sagitta sp. and fish larvae collected biweekly (n=4 reps/site) June 2013-June 2016.

Table 6. Regression analysis of dominant copepod species (>1%) with biotic factors including other dominant copepod species and commonly occurring planktonic predators. Samples collected biweekly (n=4 reps/site) June 2013-June 2016. Predator Species p-value R2 Slope Sagitta sp. Acartia tonsa 0.95 Oithona colcarva <0.001 0.31 7.65 Parvocalanus crassirostris <0.001 0.10 5.51 Fish Larvae Acartia tonsa 0.04 0.03 75.64 Oithona colcarva 0.17 Parvocalanus crassirostris 0.07 Juvenile M. leidyi Acartia tonsa 0.20 Oithona colcarva 0.02 0.10 0.52 Parvocalanus crassirostris 0.43 Adult M. leidyi Acartia tonsa 0.45 Oithona colcarva 0.13 Parvocalanus crassirostris 0.15

DISCUSSION

Dominant Species

Within the N-IRL, copepods dominated the mesozooplankton community. Other dominant mesozooplankton groups were gastropod veligers, barnacle nauplii

(Balanidae), larvaceans (Oikopleura sp.), cladocerans (Evadne sp.), and chaetognaths (Sagitta sp.). None of these groups were as consistently abundant as copepods. The N-IRL copepod community was predominantly comprised of three species: Acartia tonsa, Oithona colcarva, and Parvocalanus crassirostris.

The calanoid copepod Acartia tonsa (Fig. 3a) is a cosmopolitan species capable of thriving in a wide range of environmental conditions (Leandro et al., 2006; Castro-

Longoria, 2003; Cervetto, 1999; Rast and Hopkins, 1990). A. tonsa has high food requirements relative to other copepods due to active swimming behavior

(Gaudy, 1974; Tiselius, 1992). An opportunistic omnivore, this pervasive species can switch between suspension feeding on phytoplankton and ambush feeding on microzooplankton according to food availability (Stottrup and Jensen, 1990;

Kiørboe, Saiz, and Viitasalo, 1996). A. tonsa is fecund, with an average of 50 eggs per female, a reproductive lifespan of 25 days, and a short development time of

8.8 days (Henle unpubl in Lonsdale, 1981; Holste and Peck, 2006; Landry, 1983).

During the daytime A. tonsa tends to aggregate near the bottom and exhibits a nocturnal daily vertical migration (DVM) (Fulton III, 1984a).

The cyclopoid copepod Oithona colcarva (Fig. 3b) is the second most abundant copepod in the N-IRL. O. colcarva is an ambush forager, feeding preferentially on ciliates and dinoflagellates (Nakamura and Turner, 1997; Zamora-Terol et al.,

2014; Saiz, 2014). Unlike A. tonsa, O. colcarva swims infrequently, drawing fewer encounters with predators such as chaetognaths (Fulton, 1984b) and M. leidyi, relative to A. tonsa (Costello et al., 1999). O. colcarva is a slow developer, requiring 18 days to reach reproductive stage. It has a low fecundity of only 3-11 eggs per female and a shorter reproductive lifespan than A. tonsa (15.4 days)

(Lonsdale, 1981; Sabatini and Kiørboe, 1994). O. colcarva has a uniform distribution throughout the water column during the daytime, but migrates at night (Fulton III, 1984a).

The calanoid copepod Parvocalanus crassirostris (Fig. 3c) is the third most abundant copepod in our surveys. It is an opportunistic particle feeder, with adults primarily grazing on nanoplankton (McKinnon et al., 2003; Pafferhöfer,

1984; Calbet et al., 2000). They display similar swimming behavior to A. tonsa, actively swimming in short rapid bursts or “jumps” (Bradley et al., 2012). P. crassirostris is a quick developer, developing from egg to adult in 6.7 days

(Johnson, 1987; Lawson and Grice, 1973). During the daytime P. crassirostris aggregates on the bottom and at night exhibits a vertical migration (Fulton III,

1984a).

Biotic Factors

Abiotic factors tend to predict species richness patterns; biotic factors such as grazing and predation are more likely to be responsible for controlling species densities (Therriault and Kolasa, 1999). Thus, algal density and composition are expected to play a large role in controlling copepod community densities. Algal composition at our sites has been shown to be variable, with diatoms playing a large role in Mosquito Lagoon and dinoflagellates play a large role in Cocoa (Fig.

4a) (Badylack and Phlips, 2004). This is consistent with what is known about the dietary preferences of the dominant copepod species at these respective sites.

Oithona colcarva, which prefers dinoflagellates and ciliates (Nakamura and

Turner, 1997; Zamora-Terol et al., 2014; Saiz, 2014), was the most abundant in

Cocoa, while Acartia tonsa, an opportunistic omnivore (Stottrup and Jensen, 1990;

Kiørboe, Saiz, and Viitasalo, 1996), dominated Mosquito Lagoon plankton (Table

1). Historically, the standing algal biomass of our sites has been shown to increase from Mosquito Lagoon to Cocoa (Fig. 4a) (Badylack and Phlips, 2004). We observed an overall increase in copepod densities across this same span of sites, which is most likely a reflection of the algal food sources.

Seasonal Patterns in Copepod Communities

Phytoplankton and ichthyoplankton of the Indian River lagoon display a degree of cyclic occurrence. Ichthyoplankton communities show consistent strong seasonal

variation, peaking during the wet season (May-October) and shifting from a high diversity in the wet season to low diversity in the dry season (Reyier and Shenker,

2007). Phytoplankton communities are not as cyclic as ichthyoplankton. Although generally phytoplankton volumes follow a seasonal cycle corresponding with lagoon nutrients, algal blooms occur during all months of the year, with large variations from year to year (Phlips et al., 2002). Nutrient concentrations vary in the lagoon with seasonal patterns of rainfall, increasing during the wet season

(May 28-Oct 16) (Phlips et al. 2002; Lascody, 2002). The highest standing crops of phytoplankton in the IRL have been observed from May to November (Badylak and Phlips, 2004). The copepod community shifts composition between the dry and wet season with the percentage of herbivorous copepods increasing during the wet season (p<0.005) when standing crops of phytoplankton are the highest and carnivores increasing during the dry season (p<0.05) when standing crops of phytoplankton are the lowest (Badylak and Phlips, 2004) (Table 3, Fig. 5).

Potential Predation Effects

Primary intraplanktonic predators in the Indian River Lagoon during this study included chaetognaths Sagitta sp., fish larvae, and the ctenophore Mnemiopsis leidyi. All exhibit substantial spatial and temporal variability in presence and abundance. Sagitta spp. and fish larvae feed preferentially on certain copepod

species (Fulton III, 1984b; Demontigny, et al., 2012) and M. leidyi is a notoriously voracious predator of many taxa (Granhag et al., 2011).

Ichthyoplankton exhibited seasonal patterns similar to copepods, peaking at the beginning of the wet season and dropping off during the dry season (Fig. 11). A previous study of N-IRL ichthyoplankton communities observed that the greatest shifts in community composition occurred during late autumn, when many taxa disappeared, and in late winter/early spring, when estuarine spawning resumed

(Reyier and Shenker, 2007). The positive correlation between fish larvae and A. tonsa across all sites suggest that, like estuarine spawning, A. tonsa population increases are driven by the increased productivity of the wet season.

The strongest of correlations of copepods to intraplanktonic predators were with

Sagitta sp.. Chaetognaths are voracious feeders with a vibratory mechanism of prey detection adapted for crustaceans such as copepods (Horridge and Boulton,

1967). Each raptorial arrow worm may consume 10-12 prey daily which equates to

30 to 64% of their body weight (Kimmerer, 1984; Rakusa-Suszczewski, 1969). It is possible that a larger population of chaetognaths will result in higher relative abundance of O. colcarva, as Sagitta sp. shows a strong preference for A. tonsa and appears to avoid less active copepod species. (Fulton III, 1984b). This might explain the positive correlations between O. colcarva and Sagitta sp.(Table 6).

When present, chaetognath densities averaged 452± 89 m-3 . At these abundances, consuming 12 copepods per day and feeding on the entire copepod community an average of 13,544 copepods per m3, they have the capacity to consume 40% of the copepod community daily. At the maximum observed densities (3062 m-3) feeding on the entire copepod community for that observed sampling, chaetognath populations theoretically could consume 87% of the copepod community daily. Chaetognath densities, feeding rates (Reeve, 1980;

Kimmerer, 1984) and prey preferences all indicate that chaetognaths as predators have the potential to greatly impact the copepod community. The absence of an obvious chaetognath effect suggests that certain assumptions may be incorrect, or there may be external factors influencing predator-prey relationship. The positive correlation between copepod and predator populations suggests both populations are being driven by a common environmental variable.

Potential predatory impacts of ctenophores vary based on the density and size structure of their populations. Feeding by adult ctenophores on mesozooplankton acts as part of a positive feedback system, reducing mesozooplankton, which eases grazing pressure on microplankton, which in turn provide food for juvenile comb jellies (Fig. 12). Abundant ctenophores have indirectly triggered phytoplankton blooms by decreasing grazer volumes (Deason and Smayda, 1982).

In contrast, the survival of larval M. leidyi is dependent on the availability and

composition of microplanktonic prey (McNamara and Lonsdale, 2014; McNamara et al., 2013). Without dual prey populations for their developmental dietary transition, M. leidyi will likely not thrive (McNamara and Lonsdale, 2014;

McNamara et al., 2013) (Fig. 12). When M. leidyi is abundant, high predation rates on dominant grazers can shape the trophic web and succession outcomes.

Figure 12. Mnemiopsis leidyi feedback cycle resulting from stage-dependent behavior (adapted from McNamara et al., 2013)

Historically B. ovata and M. leidyi densities within the northern IRL peak in winter and early spring (Reyier and Shenker, 2007). This was consistent with peaks observed in December-March and June-July (all sites) (Fig. 10). Spatial and temporal patterns of M. leidyi abundance were also consistent with previous studies, with surges in population densities occurring at the northernmost site

(Mosquito Lagoon) and far lesser densities of M. leidyi at the southernmost site

(Cocoa) (Fig. 10) (Reyier et al., 2008). Juvenile M. leidyi (<1cm) occurred more frequently in northern sites, but were rarely collected in Cocoa samples. Densities of M. leidyi have previously been observed to be highest in the Banana Creek region (east of Titusville) of the NIRL. It is likely that M. leidyi is reproducing in this area and then spreading outward (Reyier et al., 2008).

M. leidyi uses 2 different processes to capture its prey: 1. it creates a flow past its oral lobes by beating its cilia and captures prey via flow entrainment; or 2. it captures prey simply through contact with its oral lobes. Both processes can occur simultaneously (Waggett and Costello, 1999). Smaller or more sedentary prey such as copepod nauplii and the copepod O. colcarva are captured through the former process, but larger or more active prey such as P. crassirostris and A. tonsa are captured through the latter. Although the method of capturing copepods varies, rates of capture for A. tonsa and O. colcarva were similar in lab studies

(Costello et al., 1999). Despite the lack of selectivity by adult M. leidyi, ctenophore presence may favor the copepod A. tonsa as juvenile M. leidyi has the potential to compete more directly for food with (i.e., microzooplankton) O. colcarva. The lack of juvenile stage M. leidyi at the Cocoa site indicates that this site probably doesn’t have a stable, self-perpetuating population of M. leidyi (Fig. 10). Sporadic appearances and variable densities of M. leidyi make it unlikely that their predation drives copepod community composition.

Environmental Factors

Wet season conditions include increased overall productivity and more variable salinities. Because the lagoon is shallow and models show water masses linger at our sites (Smith, 1993; Phlips et al., 2004), heavy rainfall can stress organisms.

During the study period, salinities remained above the minimum tolerance threshold for all species (Castro-Longoria, 2003; Cervetto et al., 1999; Rast and

Hopkins, 1990) with salinities less than 20ppt only occurring rarely (Fig. 6b). All species exhibited significant negative correlations to increasing salinity (Table 4), this correlation was driven by the hypersaline conditions(>35ppt) from July 2013 to August 2014. All the dominant copepod species are known to be able to survive salinities up to 35 ppt, but little is known on the effects of salinity >35ppt on species metabolism and fecundity. P. crassirostris and O. colcarva exhibited a greater negative response to increasing salinities than the more robust A. tonsa.

The range of temperatures that occurred during our sampling period (11-32°C) was within the optimal ranges for the dominant species (Leandro et al., 2006;

Lonsdale, 1981; Peterson, 2001). With the low seasonal variation of temperatures in the N-IRL (Fig. 6a) temperature did not play a significant role in controlling or shaping copepod communities.

Biotic Versus Abiotic Factors

Our results indicate that of all potential factors, abiotic and biotic, copepod community composition was most closely correlated with relative chlorophyll concentrations and Secchi depth, both of which were impacted by algal bloom events. Much of the community variation observed remains unexplained by our consideration of single factors. The interaction of environmental variables as well as the non-seasonal occurrence of disruptive algal blooms could be masking more subtle driving factors for copepod communities.

Copepod Community Function

Spatial and temporal variations in the copepod community’s composition alter the role of the copepod community within the larger aquatic ecosystem, both for top- down and bottom-up trophic interactions. As dominant species shift in the dry season from an herbivore that prefers diatoms to a carnivore that prefers dinoflagellates and ciliates, the community will have less of a capacity to act as a top-down controller of diatom blooms (Table 3 and Fig. 5). Inversely, the shift in the wet season towards an herbivorous copepod that prefers diatoms will reduce the community’s impact on dinoflagellates (Table 3 and Fig. 5). Populations with higher proportions of A. tonsa have a more consistent grazing impact, regardless of phytoplankton make-up, because of their mixotrophic strategy (Table 3 and

Fig.5).

Copepods form a critical link between primary production and higher trophic levels in many aquatic systems (Sommer and Stibor, 2002). Seasonal variation in copepod abundance will impact higher trophic levels. The difference in feeding behaviors in A. tonsa and O. colcarva impacts the ability of predators to capture them. The ambush feeding style of O. colcarva means that it is a more sedentary species than P. crassirostris, making it harder to detect for vibration-sensing predators. The dry season shift towards O. colcarva would increase the energetic cost of feeding for predators and could even act as a limiting factor for some species of larval fish and chaetognaths.

Another element of the copepod community that is altered by changes in species composition is the resiliency and fecundity of the species. In large bloom events, such as the one in 2015/2016, copepods can suffer heavy declines (Fig. 9). A population’s recovery time influences the degree of impact on secondary consumers such as larval fish. Wet season populations comprised of A. tonsa and

P. crassirostris likely will recover their population densities quicker from algal blooms because of their increased fecundity and faster development time. Dry season populations with a large proportion of O. colcarva will take longer to recover because of its lower fecundity and slower development (Lonsdale, 1981;

Sabatini and Kiørboe, 1994).

CONCLUSIONS

The Indian River Lagoon mesozooplankton community is largely comprised of three species of copepod. The dominance of these species makes their trophic strategies, tolerances, and behaviors important in shaping the functionality of the mesozooplankton community. The dominant species, Acartia tonsa, Oithona colcarva, and Parvocalanus crassirostris, have distinct trophic strategies which work best with particular prey communities. Change in algal dominance as a result of seasonal and spatial variations potentially drives shifts in copepod populations, particularly herbivorous species.

Copepod communities in the N-IRL appear to be regulated more from the bottom- up than the top-down. Intraplanktonic predators showed little impact on copepod densities or make-up. Variances in copepod community composition were more closely correlated with relative chlorophyll levels and water transparency than predation factors. Under bloom conditions, the densities of P. crassirostris decreased substantially. There was a seasonal shift in copepod community composition with P. crassirostris being more abundant in the wet season and O. colcarva being more abundant in the dry season. Seasonality in the N-IRL is subtle and easily overwhelmed by hypersaline conditions or dense harmful algal blooms.

This may prevent copepod communities from displaying correlations with subtle

seasonal variables. Despite this, densities and composition of the community appear to be driven from the bottom up.

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APPENDIX: Average Densities of Dominant Copepod Species by Season and Year

A. tonsa O. colcarva P. crassirostris Site Season Mean 1 S.E. Mean 1 S.E. Mean 1 S.E. Mosquito Summer 2013 3071 1158 146 97 4 2 Mosquito Fall 2013 7729 2773 410 228 32 10 Mosquito Winter 2013 822 346 98 25 25 4 Mosquito Spring 2014 4398 3985 1221 1027 302 283 Mosquito Summer 2014 6058 2068 2865 951 7252 1940 Mosquito Fall 2014 3481 852 4922 2391 5257 1869 Mosquito Winter 2014 5097 1248 986 126 196 93 Mosquito Spring 2015 2614 336 1570 831 704 233 Mosquito Summer 2015 6198 832 3433 956 5551 1864 Mosquito Fall 2015 8005 2414 2881 725 1511 590 Mosquito Winter 2015 2762 622 1589 292 42 23 Mosquito Spring 2016 2331 663 2289 1295 7 4 Titusville Summer 2013 6442 2181 788 476 17 15 Titusville Fall 2013 3484 2670 174 81 2 2 Titusville Winter 2013 575 360 110 68 35 26 Titusville Spring 2014 2530 2334 1720 1595 46 45 Titusville Summer 2014 4839 1336 2798 495 7907 4410 Titusville Fall 2014 1545 328 3182 1270 7902 1545 Titusville Winter 2014 6529 1673 7281 4235 2370 1328 Titusville Spring 2015 8925 3829 8760 3885 2202 717 Titusville Summer 2015 7399 1120 2690 860 12698 2831 Titusville Summer 2015 23391 16168 2190 369 7838 4612 Titusville Winter 2015 3457 1522 5110 1831 24 12 Titusville Spring 2016 2008 691 2353 838 1 1 Cocoa Summer 2013 16092 6715 361 119 3 3 Cocoa Fall 2013 1722 676 326 54 6 3 Cocoa Winter 2013 431 266 47 23 4 4 Cocoa Spring 2014 8240 3028 1844 669 119 5 Cocoa Summer 2014 9562 1222 5171 2065 638 166 Cocoa Fall 2014 11079 873 10200 9251 13439 7133 Cocoa Winter 2014 25655 21559 15897 11928 788 339 Cocoa Spring 2015 7793 4441 23330 12149 16943 14986 Cocoa Summer 2015 5226 860 5530 3492 39757 15545 Cocoa Fall 2015 6595 3499 5148 1564 13347 3325 Cocoa Winter 2015 7227 3221 3384 1542 38 38 Cocoa Spring 2016 4531 463 9893 8506 411 411