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Hydrobiologia

, Volume 803, Issue 1, pp 173–187 | Cite as

Modeling local effects on propagule movement and the potential expansion of mangroves and associated fauna: testing in a sub-tropical lagoon

  • John F. Hamilton
  • Richard W. Osman
  • Ilka C. Feller
MANGROVES IN CHANGING ENVIRONMENTS

Abstract

Local effects on the rates of spread of mangrove and associated epifauna were modeled for the Indian River Lagoon, Florida, USA. The model divided the 200-km-long lagoon into 157,330 cells. Data from a hydrodynamic model were used to generate current vectors for each cell at 10-min intervals. Each cell was assigned a habitat type, and releases or recruitment of mangrove propagules or epifauna larvae were based on the suitability of these habitats. Multiple species were included in the model, each with its own life-history parameters. All individuals were followed over 8 years or until mortality occurred. Adults could reproduce and release new larvae or propagules. The mean rates of spread predicted by the model were <1 km year−1 for all species, which were less than the 2 km year−1 predicted for mangroves along this coast. Spread rates were also found to differ among the five inlet source sites used in the model. Epifaunal invertebrate populations spread at similar rates, but spread more rapidly from mangrove habitats than from dock habitats. These results demonstrate that local differences in hydrodynamics and habitat distributions influence the broader regional rates of spread likely to occur with climate change.

Keywords

Climate change Range expansion Mangroves Epifauna Modeling 

Introduction

With climate change, the potential poleward shift of many species seems likely and has been predicted in many studies (Engle & Summers, 1999; Occhipinti-Ambrogi, 2007; Burrows et al., 2011; Chen et al., 2011; Doughty et al., 2016). Coastal marine and estuarine systems are no exception (e.g., Engle & Summers, 1999; Doughty et al., 2016) but local extinction of some species may also occur (Helmuth et al., 2002). Since these systems can be dominated by several critical habitat-forming species such as seagrasses, salt marshes, and mangroves (Cavanaugh et al., 2015), the impacts of changes in the distribution of these species can have broad ecosystem effects. The potential influence of climate change on the poleward expansion of mangroves is particularly important (Cavanaugh et al., 2014), as mangroves are likely to replace salt marshes with many associated species also likely to change.

Associated organisms that seem most likely to expand with mangroves are epifaunal or fouling species that usually require hard structure on which to live (e.g., Farnsworth & Ellison, 1996; Aquino-Thomas & Proffitt, 2014; Guerra-Castro & Cruz-Motta, 2014). This hard structure is generally lacking in salt marshes but is present in mangrove habitat, particularly as the prop roots of Rhizophora mangle L. Diverse epifaunal communities can contain 10 or more invertebrate phyla (e.g., Osman, 1977, 2015; Sutherland, 1980). The majority of these species are sessile and attached to the substrate as adults. Their life histories are thus similar to the mangroves in having planktonic larvae that are dispersed by water currents similar to mangrove propagules. Because they are attached as adults, their spread is largely dependent of larval transport just as mangroves are dependent on the similar transport of propagules.

The potential poleward spread of mangroves along the eastern coast of the USA has been examined and modeled by Cavanaugh et al. (2015), who projected a rate of northward expansion of <2 km year−1. However, as they stated, these projections are, in part, subject to local hydrodynamic conditions that might influence the rate at which propagules can be transported. Although many factors associated with climate change such as freezing (e.g., Lonard & Judd, 1991; Everitt et al., 1996), interactions with salt marshes (e.g., Osland et al., 2013; Armitage et al., 2015; Peterson & Bell, 2015), severe weather events, and sea level rise (e.g., Woodroffe, 1990; McKee et al., 2007; Peterson & Bell, 2015) can influence spread, the goal of this study was to examine how the hydrodynamics of one local system, the Indian River Lagoon (IRL) extending more than 200 km along the east coast of Florida, USA, might influence the spread of both mangroves and associated epifaunal species. Presently, mangroves exist throughout the IRL and farther north but in the late nineteenth century, Evermann & Bean (1897) reported mangrove “bushes” only in the southern IRL. Biomarker evidence suggests increases in mangrove abundance in Florida Bay from 1830 to the 1980s (Xu et al., 2007) and Krauss et al. (2011) found a 35% increase in mangroves in southwestern Florida from 1927 to 2005. Thus, the model focuses on how existing local hydrodynamics might have influenced similar historical changes in the IRL and potential spread rates rather than predicting any actual change in distribution with climate change. Our approach was to use output of an existing hydrodynamic model for the IRL (Davis, 2001; Sheng et al., 2002), coupled with a habitat distribution map, and an individual-based ecological model (modified from Hamilton, 2005; Supplementary Data). This model incorporates life-history characteristics for multiple species of mangroves and epifaunal invertebrates and projects their distribution within habitats of the IRL over multiple years.

We addressed several questions using this model. First, we examined how rapidly mangroves could spread, and whether this varied as a function of propagule longevity. Secondly, we examined how rapidly epifaunal species could spread and whether this varied with larval longevity and season of reproduction. Thirdly, we examined whether the introduction of anthropogenic hard structures such as docks, jetties, etc. could influence the effect of spreading mangrove habitat on epifaunal spread.

Methods

The IRL (Fig. 1) is over 200 km in length and composed of three connected bodies of water; the Mosquito Lagoon, the Banana River, and the Indian River Lagoon proper. There are five inlets to the Atlantic Ocean. From north to south, the inlets are Ponce de Leon at New Smyrna, Canaveral at Port Canaveral, Sebastian, Fort Pierce, and St. Lucie. Although there are a number of small rivers entering the lagoon, the hydrodynamics are mainly tidal with water exchange occurring mostly through the inlets and wind-driven farther from the inlets (Pitts, 1989; Smith, 1990; Liu, 1992). At present, mangroves dominate intertidal habitat throughout most of the IRL with salt marsh increasing to the north. The IRL is fairly shallow with a mean depth of <2 m (Steward et al., 2005). It has been modified by dredging a channel along much of its length as part of the much larger Atlantic Intracoastal Waterway. Numerous spoil islands were created as part of the dredging. The shoreline has been highly modified by both commercial and residential development with the hardening of the shore in many locations. The IRL with its great length and few inlets for the introduction of new species is an ideal semi-closed system for examining the effects of local conditions on the rate of spread of new species. Our approach in modeling this spread was to use the five inlets as replicate points of introduction, each with a founding population producing new propagules that could recruit to other sites within the IRL.
Fig. 1

Indian River Lagoon. Model domain showing habitats. Insets show the location in Florida, USA and the Sebastian Inlet area with details of habitats

The mangrove and invertebrate species in the IRL have a broad array of life-history traits. In particular, the mangrove species are long-lived, with individuals often living many decades and their propagules surviving in the water for weeks to months (e.g., Rabinowitz, 1978a, b; McKee, 1995a). The majority of invertebrates are generally short-lived, existing for months to only a few years and have larval longevities in the water from hours to only a few weeks. Thus, these species represent a broad range of times in which recruiting individuals (propagules or larvae) can be distributed by local hydrodynamic processes. Although invertebrate larvae differ from floating mangrove propagules in having some mobility, we have assumed that in the shallow IRL this did not influence their distribution. In this study, our focus was on the potential differences between propagule or larval longevity and time of reproduction. Therefore, we modeled two mangrove species as differing only in the propagule survival times, 60 days (nominally Rhizophora mangle) and 20 days (nominally Avicennia germinans (L.) Stearn) and reproductive season (Table 1). We also modeled three epifaunal invertebrates, two with a larval longevity of less than a day (ascidians, bryozoans) to one with longer-lived larvae of a week or more (barnacles). The two species with short-lived larvae differed in producing larvae in the winter (bryozoans) or summer (ascidians).
Table 1

Model variable values used

Stage

Variable

Rhizophora

Avicennia

Ascidian

Bryozoan

Barnacle

Propagule

Loss probability (d−1)

0.05

0.05

   

Maximum lifetime (d)

60

20

   

Settlement prob. (d−1)

0.10

0.10

   

Release months

6–9

7–10

   

Recruits

Loss probability (d−1)

0.005

0.005

   

Maximum lifetime (d)

160

160

   

Juveniles

Loss probability (d−1)

0.002

0.002

   

Maximum lifetime (d)

320

320

   

Adults

Loss probability (d−1)

0.001

0.001

   

Maximum lifetime (d)

None

None

   

Larva

Loss probability (ts−1)

  

0.05

0.05

0.05

Release time of day

  

Day

Day

Day/night

Settlement prob. (ts−1)

  

0.01

0.01

0.01

Release months

  

6–9

1–5

2–11

Maximum age (h)

  

6

6

12

Recruits

Loss probability (d−1)

  

0.02

0.02

0.01

Maturation age (d)

  

7

14

7

Juvenile

Loss probability (d−1)

  

0.005

0.005

0.005

Initial space (cell)

  

0.003

0.003

0.005

Growth rate (d−1)

  

0.025

0.025

0.025

Maturation age (d)

  

14

14

14

Adults

Loss probability (d−1)

  

0.003

0.003

0.005

Growth rate (d−1)

  

0.025

0.025

0.025

Max longevity (d)

  

60

60

None

Probabilities were applied to all individuals of the life stage at the end of each model day (d−1) or at the end of each model time step of 10 min (ts−1). Initial space assigned to juveniles was in proportion of a model cell (cell)

The model is an individual-based model that simulates the life cycle of mangroves and epifaunal invertebrates from propagule/larval release, their transport by water flow, recruitment into suitable habitats, and growth into juveniles and then mature adults, with provisions for mortality at all of these stages (Hamilton, 2005, see Supplementary Data for a detailed description of the model). Adults can become reproductive and release new propagules/larvae. The model uses the output from an existing hydrodynamic model of the IRL (see below) to drive propagule and larval movement. The model includes extensive menus that allow the user to define habitats and habitat distribution, life-history attributes for multiple life stages of each species included, habitat use for each species, and disturbance rates and intensity for defined regions and habitats of the IRL (the model is available upon request).

Domain

The model domain consists of the portion of the IRL extending from Ponce de Leon Inlet in the north to St. Lucie Inlet in the south, and includes small extensions offshore of the inlets (except Canaveral) that lead to the Atlantic Ocean (Fig. 1). This model domain was divided into a grid of square cells, each 100 m on a side, resulting in 157,330 cells within the model domain. Each cell was assigned a habitat type, representing the majority of the habitat within that cell. Initial habitat designations were based on estimates of present habitats using charts, maps, and satellite images (e.g., Google Earth). Habitat types were designated as allowing propagule or larval settlement (suitable habitat) or prohibiting settlement (unsuitable habitat) as well as whether they were suitable for reproduction and propagule/larval production. Separate habitat designations suitable for each species were included in a model run. Habitats suitable for invertebrates were all hard substrate habitats (mangroves, docks, oyster reefs). Habitats designated available for mangroves included beaches, marshes, oyster reefs, and mangroves.

Species

All species had four life stages and each individual of a species transitioned through these. These life stages are as follows:
  1. (1)

    A propagule or larva, which was released from a reproductive adult in the appropriate habitat. The currents generated by the hydrodynamic model distributed individuals in this stage.

     
  2. (2)

    A propagule or larva transitioned to a recruit immediately after settlement into an appropriate habitat. An individual remained in this stage for a short period after which it grew into the next stage.

     
  3. (3)

    After the recruit stage, an individual transitioned to a juvenile, which was a pre-reproductive stage. The length of this stage was defined for each species (Table 1), usually weeks to months.

     
  4. (4)

    Finally, an individual transitioned to an adult after the juvenile stage. In this stage, individuals were reproductive and could release propagules or larvae. The length of this stage was defined for each species (Table 1) but could be for multiple years.

     

All life stages had a set of life-history parameters that could be varied for each species and controlled for mortality, growth, length of the stage, reproduction, and probability of entering the next stage. Table 1 shows these variables and the values used in the model for this study (any or all of these values can be changed by the user). Propagule and larval production rates were simplified to one for each adult per model time step during the defined reproductive period of each species.

Hydrodynamics

Much of the Indian River Lagoon system is within the St. Johns River Water Management District of northeast Florida, USA. The District kindly supplied us with four years of output of their hydrodynamic model, which they use for studying water flow and related issues. The hydrodynamic model in use is the CH3D model originally developed by Sheng (1990a), further developed by Davis & Sheng (2000), and specifically applied to the IRL (Davis, 2001; Sheng et al., 2002). The complete mathematics of the hydrodynamic model, an extensive literature review, and comparisons to Indian River Lagoon field measurements are all provided by Davis (2001). Sheng (1990b) also provides additional information on validation of the model and its use in other water bodies. For the Indian River Lagoon, hydrodynamic model output data for 4 years (1999–2003) were used. In general, each propagule transport model run was 8 years in length, using the same hydrodynamic data for each of two successive 4-year periods. Each time step of a model run was 10 min, and at each time step current vectors were generated for each cell. Every propagule or larva within each cell of the model domain was moved in accordance with the water velocity in that cell. If a propagule was within a cell of suitable habitat, then settlement could take place with a specified probability, resulting in a new recruit at that location. A recruit proceeded to grow at a specified rate and subject to mortality, through a juvenile and then an adult stage. Adults could release new propagules or larvae of their own in a defined reproductive season.

Model parameters

For each of the model runs in this study, we used the life-history parameters in Table 1. The two mangrove species differed in the maximum length of their propagule life stage and the months in which propagules were released. Rhizophora propagules had a 60 days maximum lifetime and were released June–September. Avicennia propagules had a 20 days maximum lifetime and were released July through October. Probabilities such as mortality and settlement were applied to all individuals of all appropriate life stages at the end of each day. Three invertebrate taxa were used, including a colonial bryozoan, a colonial ascidian, and a barnacle. The bryozoan and ascidian had a relatively short larval period of approximately 6 h or one-half a tidal cycle. They differed in that the bryozoan was reproductive and released larvae in the winter/spring (February–May) and the ascidian was reproductive in the summer (June–September). The barnacle differed in having a longer larval period of approximately 12 h and it released larvae in all months except November–December. It also released larvae for 24 h each day while the ascidians and bryozoans released larvae for 12 h from 0600 to 1800. These values were based on recruitment data collected in the IRL at Fort Pierce since 2005 and known general life histories for each taxon. Probabilities were applied to all individuals of the larval life stage at the end of each 10-min model time step and to all individuals of the recruit, juvenile, and adult life stages at the end of each day.

Habitat designations for mangrove recruitment and reproduction were beach, marsh, oyster reefs, and mangroves. Habitats designated for invertebrate recruitment and reproduction were mangroves, docks, and oyster reefs.

Separate 8-year model runs were done for mangroves and invertebrates. For the mangrove runs, we changed all existing mangrove habitat to either beach or marsh. At each inlet, we assigned 5–10 cells to mangrove habitat with small founding populations. Because docks were not suitable for mangrove recruitment, cells with dock habitat were no different than other unsuitable habitat such as subtidal sediments and seagrasses. We conducted five replicate runs for founding populations at each of the five inlets. For invertebrate runs, we used approximations for existing mangrove and dock habitat distributions derived from charts, aerial photographs, and satellite images (Google Earth). However, we assigned the same initial inlet source areas as were used in the mangrove runs. Again, separate runs were done for each inlet.

Distribution data were collected at the end of 4 and 8 years. For each taxon, we combined recruit, juvenile, and adult life stages present in each cell. The distance to the source inlet for each of these individuals was calculated and used for analyzing mean, median, and maximum spread rates as well as the overall distribution of individuals relative to the source inlet.

Results

Mangrove expansion rate from inlets

In the model, the two mangrove species differed only in their propagule longevity and season of propagule release. Rhizophora propagules were released June through September and remained viable for 60 days. Avicennia propagules were released July through October and were viable for 20 days. Based on the results of 25 model runs of 8 years each, the differences between the two species were fairly small. Table 2 contrasts the two species for each life stage as well as the total number of individuals of all stages (because the model ended in the winter no propagules were present). After 4 years, there was no significant difference (F = 0.018, P = 0.894) in the mean distance that both species spread (Rhizophora = 3.19 ± 0.04 km, Avicennia = 3.18 ± 0.03 km), but after 8 years the mean distance of Avicennia (7.83 ± 0.01 km) spread was significantly greater (F = 310,178, P < 0.0001) than Rhizophora (5.77 ± 0.01 km). As can be seen in Table 2, the mean distances spread for all life stages were similar to that of all stages combined with the exception of Rhizophora adults (2.85 ± 0.07 km) and juveniles (2.88 ± 0.08 km) spreading slightly but significantly farther (F a = 9.5, P < 0.002, F j  = 5.3, P < 0.02) after 4 years than those of Avicennia (2.54 ± 0.06, 2.64 ± 0.07 km). Median spread was similar to the mean rate of spread but for all stages the maximum rate of spread for Rhizophora was greater than the spread of Avicennia. In general, the rate of spread of both species from their inlet sources ranged from 1.1 km year−1 for Avicennia recruits after 8 years to 0.63 km year−1 for Aviciennia adults after 4 years.
Table 2

Model output spread rates for stages of mangrove

Years

Species

Stage

Mean

SE

Max

Median

4

Avicennia

Adult

2.54

0.06

16.70

2.38

Juvenile

2.64

0.07

21.51

2.28

Recruit

3.41

0.04

24.73

3.10

All

3.18

0.03

24.73

3.18

Rhizophora

Adult

2.85

0.07

29.16

2.42

Juvenile

2.88

0.06

27.33

2.39

Recruit

3.42

0.05

37.62

2.91

All

3.19

0.04

37.62

3.01

8

Avicennia

Adult

6.64

0.01

38.46

9.33

Juvenile

7.48

0.01

33.08

9.05

Recruit

7.95

0.01

47.38

9.93

All

7.83

0.01

47.38

9.88

Rhizophora

Adult

5.01

0.01

55.40

9.01

Juvenile

5.70

0.01

63.07

8.81

Recruit

5.89

0.01

55.54

10.04

All

5.77

0.01

63.07

10.11

The rate of spread of all life stages from the five inlet source areas differed significantly over 4 and 8 years (Fig. 2; Table 3). Although the ranking of the inlets differed somewhat among the species and life stages, the general pattern is that spread was lowest from the inlets at the southern (St. Lucie) and northern (Ponce) ends of the IRL. This is most evident after 8 years. The Sebastian Inlet exhibited the highest spread rates, being three times the rate from the St. Lucie Inlet. The St. Lucie Inlet is dominated by the St. Lucie River that generates high currents through the inlet, which may impede the distribution of propagules to the north. Also, spread from the two end member inlets was restricted to mostly one direction, either north for St. Lucie Inlet or south for Ponce.
Fig. 2

Distributions of mangrove species after 4 and 8 years, based on 5 model runs for initial populations at each of the 5 inlets (5 runs/inlet). The contributions of each inlet to each distance are shown

Table 3

Comparison of spread distance from the initial populations at the five inlets

Mean distances (km) after 4 and 8 years were compared using ANOVA. Letters indicate differences among the inlet sources in each of the analyses. Inlets: Can Canaveral, FP Ft Pierce, Pnc Ponce, Seb Sebastian, SL St Lucie

As can be seen in Fig. 2, the two species also differed greatly in the overall number of individuals present with Rhizophora having approximately 10 times more individuals of all life stages than Avicennia. This occurred after both 4 and 8 years across all inlet sources. For both species, the number of individuals was highest for Sebastian and St. Lucie Inlet sources and lowest for Canaveral and Ponce. The main difference between the two species in the model was the longevity of their propagules, which presumably allowed more propagules of Rhizophora to travel farther from their sources. This may contribute to the higher number of Rhizophora individuals at greater distances from Sebastian and Ft. Pierce sources but not those with the St. Lucie Inlet as their initial source. Differences among inlets and species are most likely the result of hydrodynamic and habitat distribution differences.

Expansion rates of associated fauna

All three epifaunal species were restricted to mangrove, oyster reef, and dock habitats. The mean distances spread for the three species after 4 years were similar to the two mangroves species. The distance varied from 1.8 km for bryozoans on mangroves to 5.7 km for ascidians on oyster reefs. After 8 years, distances spread did not increase greatly and remained less than that for the mangroves. The distances varied from 1.6 km for bryozoans on mangroves to 9.5 km for ascidians on docks (Table 4). The overall distributions of the three species after 8 years are shown in Fig. 3. Barnacles with the longer-lived larvae and a longer reproductive season had the largest population size and spread the greatest distance from their inlet sources. Their distribution was bimodal with a large part of the population within 5 km of the sources and a smaller component 10–15 km from the sources. Bryozoans with a winter reproductive season had a much smaller population size and spread the shortest distance. Ascidian populations were intermediate in size with a bimodal distribution with a large peak at 3 km and a much smaller peak at 16 km from the source inlets. For all three species, the number of individuals on docks was much smaller than for mangrove habitat. Maximum distances spread for all three species were lower than the spread of the two mangrove species with barnacles spreading the greatest maximum distance of 21 km and bryozoans a maximum of 15 km. The distance spread on docks was similar to mangroves for ascidians and barnacles but less for bryozoans.
Table 4

Model output spread rates for invertebrate species

Years

Species

Habitat

Mean

SE

Max

Median

4

Ascidian

Mang

2.20

0.04

16

2

Dock

4.14

0.07

13

4

Oyst

5.75

0.06

17

3

Barnacle

Mang

3.06

0.01

16

3

Dock

4.94

0.02

21

6

Oyst

3.67

0.01

17

3

Bryozoan

Mang

1.79

0.01

5

2

Dock

3.78

0.09

5

4

Oyst

3.34

0.01

9

5

8

Ascidian

Mang

2.66

0.02

16

3

Dock

9.49

0.22

21

10

Oyst

5.07

0.05

17

3

Barnacle

Mang

3.97

0.01

16

3

Dock

6.96

0.02

21

10

Oyst

5.94

0.01

17

3

Bryozoan

Mang

1.64

0.02

5

1

Dock

3.79

0.13

5

4

Oyst

6.39

0.01

15

6

Means were calculated for each habitat type in which adults were found at the end of 4 and 8 years. Habitats: Dock, Mang mangrove, Oyst oyster reef

Fig. 3

Distributions of the three invertebrate taxa after 8 years. Arrows indicate the maximum distance for each species on mangroves or docks. The contributions of mangrove and dock habitat to distribution are indicated for each distance

As with the mangroves, the spread of all three invertebrate taxa varied significantly among the five inlet source sites (Table 3). However, unlike the mangroves the spread of invertebrates was significantly higher from the southern St. Lucie and northern Ponce Inlets than from the other 3 inlets with the spread from the Canaveral Inlet significantly less than from the other inlets. This inlet is the most isolated from the others and had less suitable oyster reef and dock habitat in its vicinity than the other sites. Both these habitat types were more prevalent near the St. Lucie and Ponce Inlets.

Discussion

In their review of the dispersal of both marine and terrestrial propagules (including seeds, larvae, etc.), Kinlan & Gaines (2003) found genetic evidence that suggested that dispersal distances for marine plants could be >10 and >100 km for marine invertebrates. On the other hand, directly measured dispersal distances of <100 m for marine plants and invertebrates were most common. As they discussed, this variability results from such things as differing modes of dispersal, biases associated with reporting of only successful dispersal, or taxonomic biases (e.g., most studies of marine invertebrates have focused on sessile species with short-lived larvae).

This variability in dispersal distance is also seen for mangroves and associated epifauna. Genetic evidence for Avicennia germinans (Nettel & Dodd, 2007) indicates the possibility of long-distance dispersal across the Atlantic Ocean, and Clarke (1993) found long-distance dispersal distances for Avicennia marina (Forsk.) Vierh. of 50 km. However, based on propagule physiology, de Lange & de Lange (1994) argued that A. marina in New Zealand dispersed only short distances, and in a short-term tracking experiment de Ryck et al. (2012) found that the maximum dispersal distance was <200 m. On the other hand, Stieglitz & Ridd (2001) found that mangrove propagules could be transported up the Normanby estuary in NE Australia at rates greater than 3 km day−1. Although transoceanic transport of marine invertebrate larvae can occur (e.g., Scheltema, 1974, 1986a, b) and the long-lived larvae of barnacles and most molluscs and crustaceans are likely transported long distance along coasts (e.g., Caley et al., 1996; Shanks et al., 2003), many common epifaunal species such as ascidians and bryozoans have short-lived larvae that are dispersed <10 m (e.g., Olson, 1985; Davis & Butler, 1989; Osman & Whitlatch, 1998).

Given the variation in dispersal for both mangroves and associated epifaunal marine invertebrates, we examined the potential spread of these taxa within one coastal system, the IRL. Our study used an individual-based model (see Supplementary Data) that was driven by output from an existing hydrodynamic model. We initiated the model with small populations at each of the five inlets of the IRL. These populations were assumed to represent founder populations that could spread given favorable environmental conditions. Given that mangroves and the associated fauna already exist throughout the IRL, these conditions are already present. Thus we are using the IRL and the existing hydrodynamic model to represent how spread in a new region might be influenced by local conditions or how mangroves might have spread historically after an initial introduction.

It is important to note that our model focused only on the influence of local hydrodynamics and there are other processes that can influence the recruitment and spread of both mangroves and epifauna. For mangroves, freezing (e.g., Pickens & Hester, 2011, Cavanaugh et al., 2014), sea level change (Nettel & Dodd, 2007), predation on propagules (McKee, 1995b; Sousa & Mitchell, 1999; Delgado et al., 2001), and interactions with saltmarshes (Stevens et al., 2006; Pet erson & Bell, 2015) have been shown to influence spread. For epifauna, weather (Balch et al., 1999), rafting (e.g., Worcester, 1994; Thiel & Haye, 2006; Bryan et al., 2012), predation on settling larvae (Young, 1988; Young & Cameron, 1989; Bullard et al., 1999) and recruits (Osman et al., 1992; Hunt & Scheibling, 1997; Osman & Whitlatch, 1998, 2004), and resident communities (e.g., Grosberg, 1981; Ambrose & Nelson, 1982; Havenhand & Svane, 1989; Holloway & Keough, 2002; Arnold et al., 2010) can all influence dispersal and spread.

There are several other features of the model that should be taken into account in the interpretation of the results. First, we have tried to use life-history parameters for the different species that were representative of known parameters. We focused mostly on parameters affecting propagules and larvae. Propagule (e.g., Rabinowitz, 1978a, b; Drexler, 2001; Allen & Krauss, 2006) and larval longevity (e.g., Davis & Butler, 1989; Todd, 1998; Marshall & Keough, 2008) were varied among species. Release times of mangroves were set to summer and early autumn to enable peak recruitment in the autumn (Parkinson et al., 1999; Donnelly & Walters, 2014) with longer-lived Rhizophora propagules being released earlier. Larval release times were based on our monitoring of recruitment and known seasonal distributions (e.g., Weiss, 1948; Mook, 1980). Other parameters were held constant between the two mangrove species or among the three invertebrate taxa. As would be expected, mortality rates decreased and longevities increased from the youngest to oldest life stages (Table 1). It is likely that changes in the parameter values used could influence the overall rates. For mangroves, we allowed individuals to reach an adult stage within one year with consequent propagule production possible. Although precocious reproduction has been observed in mangroves (Dangremond & Feller, 2016), this early reproduction is not likely to occur for all, or even a significant number, of individuals. However, it is more likely at the edges of spreading populations (Dangremond & Feller, 2016). Using this early reproduction was done for the practical convenience of allowing results to be obtained after 4 and 8 years of model runs. For associated fauna, the maximum larval life for barnacles was somewhat shorter than generally observed (e.g., Anil et al., 2010; White et al., 2014) which may have influenced their spread rate. Additionally, the model results were potentially influenced by the distribution of habitats used. Although the initial habitats assigned to cells were based on presently observed distributions, they still remain one of many possible representations. As stated in the methods, mangrove habitat was converted to beach or salt marsh habitat for the mangrove runs. The results most likely to be influenced by the habitat distributions used were contrasts among inlet sources for invertebrate runs. If more appropriate habitats were located within the range of larval distribution from a particular source, it is likely that populations could expand more rapidly from that inlet. Finally, weather, particularly the importance of wind on water movement (Pitts, 1989; Smith, 1990; Liu, 1992), was not included in the model. Again, model results should be viewed as representing potential influences on spread rates rather than absolute rates.

Mangrove Spread

The rate of spread of both mangrove species in the IRL was similar and 0.6–0.9 km year−1 over 4 years and 0.7–1.1 km year−1 over 8 years. This is less than half the potential rate projected for mangroves along this coast (Cavanaugh et al., 2015). The distribution of adults in terms of distance from the initial inlet sources was also similar for both species after both 4 and 8 years (Fig. 2). After 4 years, the distribution of adults of both species had skewed distributions with a peak 1–2 km from the initial sources. There were also much smaller clusters of adults 6–8 km from the sources. After 8 years, both species exhibited bimodal distributions with peaks at 1–2 and 8 km from the inlet sources. This suggests that the small clusters of adult mangroves at 6–8 km found after 4 years were able to expand, much as the initial inlet populations had.

The differences among inlets are also reflected in Fig. 2 and Table 3. The Ponce and Canaveral populations had distributions similar to the overall distribution but their population sizes were much smaller than those at the other three inlets. The other three sites differed in that the St. Lucie population remained clustered near the inlet while the Fort Pierce population peaked at 6 km and the Sebastian population at 9 km. These differences demonstrate the variation in local effects. The St. Lucie Inlet is dominated by the St. Lucie River, which influences the tidal currents. This appears to slow the rate at which propagules can be carried beyond the inlet. The spread at the Ft. Pierce and Sebastian Inlets may also be influenced by the distribution of habitats near them as well as the ability for populations to expand both north and south in the IRL.

The similarity in the distribution of both species suggests that the difference in their propagule longevities had little influence on their mean rates of spread. However, Rhizophora with its greater propagule longevity did have a maximum spread of 63 km (32 km for Canaveral to 63 km for Ft. Pierce) over 8 years while Avicennia spread a maximum of 38 km (17 km for Canaveral to 38 km for Sebastian). Given the ability of small populations of both species to expand rapidly, individuals at these maximum distances may contribute to a more rapid spread over longer time intervals.

Finally, if mangroves were only in the southern IRL in the late 1800s (Evermann & Bean, 1897), then their range expansion to the entire IRL might be assumed to be 100–200 km in a period of <100 years. Thus, the ~1 km year−1 rate of mangrove spread predicted by the model is certainly within the range of spreading rates based on historical data. The range of potential spread in the IRL for both species also falls within the range of short (e.g., de Lange & de Lange, 1994; de Ryck et al., 2012) and long distance (e.g., Clarke, 1993) spread previously reported for mangroves.

Epifaunal Spread

The spread distances of the three epifaunal taxa were contingent on the distribution of suitable habitat, which included manmade structures (docks), mangroves, and oyster reef. We examined their spread using approximations of the present distributions of these habitats. In addition, the longevities of larvae of these taxa were also much less than mangrove propagule longevities. Nevertheless, the spread of these species over the first 4 years of model runs was not much different than for the two mangrove species (Table 4). Rates ranged from 0.45 km year−1 for bryozoans on mangroves to 1.4 km year−1 for ascidians on oyster reef. However, over 8 years the invertebrate spread did not increase greatly and rates were generally lower than those for the two mangrove species. Except for ascidians on docks (1.2 km year−1 based on a small population of 75 surviving individuals), they ranged from 0.9 km year−1 for barnacles on docks to 0.2 km year−1 for bryozoans on mangroves. The limited spread of the invertebrates in contrast to the mangroves can be seen in the maximum distances spread which ranged from 5 to 21 km over 8 years.

The differences among the three species were not that great (Fig. 3). Barnacles with greater larval longevity and a longer reproductive season did develop a larger population as well as showed a bimodal distribution similar to that seen for the two mangrove species with peaks at 2 and 11 km from initial source populations. Overall both ascidians and bryozoans had populations concentrated within 10 km from the source sites. Bryozoans, which were reproductive in the winter/spring had the smallest population sizes and had the lowest rates of spread. Although the rate of spread for barnacles is within dispersal ranges previously reported (e.g., Caley et al., 1996; Shanks et al., 2003), the predicted distances for bryozoans and ascidians are generally greater than often reported (e.g., Olson, 1985; Davis & Butler, 1989; Osman & Whitlatch, 1998). However, the 8-year time frame of the model was much greater than the short hours to weeks observation periods of most studies of these species.

The greatest difference seen for all three invertebrate species was the much lower numbers on dock habitat (Fig. 3). Although dock habitat existed throughout the model IRL, it occupied many fewer cells and was much more dispersed than mangrove habitat. This is the clearest demonstration that habitat distribution can influence model results and the rates of spread.

Effects of local dynamics and disturbances

Overall the model results indicate the potential for local dynamics to influence the rate at which mangroves and associated species can spread into regions and habitats where they do not exist. If mangroves are estimated to be spreading poleward at a rate of 2 km year−1 (Cavanaugh et al., 2015), the mean rates observed for both mangrove species and associated invertebrate taxa in the model indicate that this rate can be greatly reduced by the interaction of local currents carrying propagules and larvae with the longevities of these distributional stages. However, the maximum distances that adults were observed after 8 years also suggest that spread rates could actually exceed 2 km year−1, assuming that environmental conditions were favorable for recruitment. In addition to the overall rates of spread, the differences in the rates of mangrove spread from the different inlet source sites and the differences between mangrove and dock habitat for the invertebrate taxa demonstrate that spread can be influenced on a much more local level. Differences in hydrodynamics and habitat can slow or increase spread rates.

Although the model includes the capability to examine the effects of mortality resulting from disturbance at different magnitudes and spatial scales, we did not include disturbance in any of the model runs. Our rationale was that based on the degree of spread from very small founding populations at each of the inlets, it was clear that as long as a disturbance or a series of disturbances did not cause complete local extinction, the species as modeled should be able to recover. However, major disturbances such as hurricanes (e.g., Proffitt et al., 2006; Jiang et al., 2014) could cause major losses as well as greater dispersal of propagules. Spread rates can be influenced by such events but any spread that might occur with climate change should also continue.

In conclusion, the modeling presented here suggests that local dynamics and habitat distributions can influence the rates at which species’ ranges expand with climate change that creates an environment favorable for this expansion. The slower rates observed in our modeling than the projected rate of 2 km year−1 suggest that local conditions can limit the rate of spread. However, the spread will continue. Finally, the life-history parameters used may have actually resulted in higher rates of spread for at least the mangroves. Nevertheless, at least for the 200-km-long IRL, the modeling suggests a fairly rapid expansion of mangroves and associated fauna in terms of both distance spread and the size of local populations.

Notes

Acknowledgements

We gratefully acknowledge the support of this research by grants from the NSF MacroSystems Biology program (EF1065821) and the NASA Climate and Biological Response program (NNX11AO94G). This is Smithsonian Marine Station at Fort Pierce Contribution No. 1063 and TMON Contribution No. 15. We are also grateful to David Christian, Peter Suscy, and Troy Rice of the St. John’s River Water Management District of Florida for providing output of hydrodynamic model data that were used in our model.

Supplementary material

10750_2017_3231_MOESM1_ESM.docx (23 kb)
Supplementary material 1 (DOCX 23 kb)

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Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of ConnecticutGrotonUSA
  2. 2.Smithsonian Environmental Research CenterEdgewaterUSA

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