Caribbean Sponge Recruitment and Growth on Coral Reef and Mangro E Sites in Belize

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2019 Caribbean sponge recruitment and growth on coral reef and mangrove sites in Belize Connor Daniel O'Halloran

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COLLEGE OF ARTS & SCIENCES

CARIBBEAN SPONGE RECRUITMENT AND GROWTH ON CORAL REEF AND

MANGROVE SITES IN BELIZE

CONNOR O’HALLORAN

A Thesis submitted to the Department of Biological Sciences in partial fulfillment of the requirements for graduation with Honors in the Major

Degree Awarded: Spring 2019

The members of the Defense Committee approve the thesis of Connor O’Halloran defended on April 25, 2019.

Dr. Janie Wulff Thesis Director

Dr. Sven Kranz Outside Committee Member

Dr. Andrew Rassweiler Committee Member

Abstract:

Sponges play important roles in supporting coastal marine ecosystem health and have been shown to have particularly important ecological significance in both mangrove and reef ecosystems where they are found abundantly. This study aims to compare how recruitment differs between these habitats by observing recruitment rate, species composition, and community dynamics on recruitment surfaces placed in each location over 3 years. This study also aims to analyze the growth rates of individuals of 4 of the most common species of

Caribbean reef sponges. This was done by measuring the same individuals of the 4 species at least annually over 5 years, while leaving them undisturbed in the field. This thesis was based on a dataset previously collected which included community composition data and size distribution data of sponges. Over 3 years, a total of 20 species and 13 species were identified on the recruitment substrata that were supplied in the reef site and the mangrove site respectively. The sponge fauna differed in all species between the two sites. Varying trends in the number of individuals recruited and total volume were also observed between sites such as a drop off in individuals in the reef site and a large increase in volume in the mangrove site over 3 years.

Growth rates differed greatly among the 4 species of Caribbean reef sponges. Large differences in sponge volume and in sponge species composition, over all the years considered in this study, in comparisons both between and within the reef and mangrove sites suggest that sponge communities may be highly dynamic.

Introduction:

Sponges (Phylum Porifera) are a group of ecologically and taxonomically diverse sessile organisms that are important to many coastal marine ecosystems. Sponges have simple but efficient body plans with specialized cells for life functions, particularly for immense filtration, but no organized tissues or organs. More interest has shifted into the study of coastal marine ecosystems because of the direct connection between ocean health and our own. This group has been shown to be much more complex and important than its deceivingly simple organization lets on. Sponges are highly efficient filter feeders and are able to displace large quantities of water relative to their size, which gives them the potential to significantly improve water quality in their environment (Perea-Blazquez et al. 2012). They also help facilitate the formation and restoration of important reef ecosystems by increasing coral survival by an order of magnitude

(Wulff, 1979). Sponges can even function as bio-indicators for the health of their environment

(Muricy, 1989). Still, there is relatively little known about sponges when compared to other organisms due to the difficulty of identifying and measuring these diverse organisms.

Specifically, sponge growth and recruitment trends must be better understood for insight into such an impactful group.

Sponge growth is quite a complex quality to study. Not only is there the logistical difficulty of performing a time series census in a marine setting, but sponges are also a diverse group. More than 20 orders of sponges are represented on coral reefs (Wulff 2017), and they can differ drastically in characteristics such as morphology and growth rate. Even within species of 5 sponge, there can be a decreased growth rate with an increase in size (Dayton 1979). While there have been some population or community level studies on Caribbean sponges (Wulff

2013), there have been fewer studies looking at the level of the individual. While community- level studies are integral to understanding a system, they have limits. Specifically, it does not differentiate between an individual sponge’s recovery rate from partial mortality, and their susceptibility to being wounded (Wulff 2006). Further, a better understanding of individual sponge growth rates may reveal trends in growth and survival that are unique to each species as well as variation within species. This part of my comparison aims to describe the long-term growth of four species of Caribbean reef sponge, focusing on the individual’s volume change.

A sessile marine organism’s colonization process can be divided into four main stages; dispersal of larvae, habitat choice, settlement, and recruitment (Keough & Downs 1982). Many biotic and abiotic factors can affect colonization success. When sponges sexually reproduce, the offspring possess a planktonic larval stage (Muricy, 1989). Even with sponges being a vital part of benthic communities, there are few studies on the recruitment of these larvae. In Caribbean species, sponges are not only important to reef ecosystems but mangrove prop root ecosystems as well. They are one of the most abundant groups found in mangrove prop roots when it comes to diversity of species as well as the amount of biomass present. (Rutzler & Feller 1996).

Interestingly, they tend to overlap very little in terms of species composition between coral reef and mangrove habitats (Rutzler et al 2000), even when in relatively close proximity. This phenomenon may be explained by spongivorous fish preventing sponges typically found on mangrove roots from colonizing reefs through predation, or reef species getting outcompeted on mangrove roots by local species (Wulff 2004). There is also evidence that larvae disperse over relatively short distances and may not consistently reach the other area (Zea 1993). For this 6 study, sponge recruitment abundance and species composition were determined over three years for typical mangrove and coral reef habitats. Those being Hidden Creek and the Blue Ground

Range, Belize respectively. These experiments aim to perform comparisons in sponge recruitment rate, volume change, and species composition between these habitats.

Materials and Methods:

Long Term Growth Analysis

Near the Carrie Bow Cay field station of the Smithsonian, a 400 m2 census plot was established on a shallow reef in June 2006. Within the Blue Ground Range, a series of cays, seven areas of reef were selected as a representative of the reef. Maps of the underwater landscape were created and every sponge, coral, and gorgonian in the census plot was drawn within. Each sponge was then identified by its respective species. Linear measurements were taken of each sponge without distressing them and the volume of each was estimated by the conglomeration of geometric solids. The census was done about yearly since 2006, and all census data was collected by Dr. J. Wulff. This project will be looking at data collected from

2013 to 2018 and focusing on four sponge species; Iotrochota birotulata, Ircinia strobilina,

Ircinia sp. A, and Verongula rigida. To analyze this data, the detailed maps of the census area will be used for analysis. Taking pictures of the sponges would not be the most accurate way of measurement because sponges are intricate 3-dimensional organisms, and taking a picture only gives you an unsatisfactory 2-dimensional view of them. (Wulff 1991). Each individual sponge will then be given a unique designation on the map. When using the word “individual”, this applies to all living material within a constant surface, since sponges can take on an innumerable amount of unique forms. For sponges with asexual fragmentation life history strategies, the term

“individual” can also mean all pieces of the individual that have broken off and settled 7 somewhere within the census area. (Wulff 1991). The volume of each designated individual will be calculated and recorded for that year. Since sponges are sessile invertebrates, they should be in the same location for the subsequent years. This enables identification of the same individuals by matching their placement on the reef of new census maps to previous ones. The compiled and analyzed data are in the form of volumetric changes of individuals recorded yearly from 2013 to

2018 with all individuals overlaid on a graph.

Recruitment

To study reef recruitment, dead coral rubble was collected, then rinsed in the rain and dried in the sun for at least a week. The pieces were then combined into piles which were stabilized by 1mm cable ties and anchored onto the reef using 18-gauge stainless steel wire. 16 piles in total were placed onto eight patch reef locations within the Blue Ground Range. These recruitment piles were then surveyed annually for sessile recruits by gently pulling apart the piles and photographing the recruits. These individuals were measured by volume and identified for species. Small (2x2x3 mm) samples were taken for identification from those where the species was uncertain.

To study mangrove recruitment, 17 PVC pipes with 2.2 cm outside diameter and 25 cm in length were suspended among mangrove roots in Hidden Creek, Twin Cays, Belize. At least yearly, every sessile individual found on each pipe was measured by volume and recorded. Each individual sponge species was identified, and small samples of individuals not able to be confidently identified were taken for identification to the lab. All data in this project was collected by Dr. J. Wulff. 8

Results:

Community Development and Recruitment

After three years, the 17 recruitment pipes in

Hidden Creek were covered in a variety of sessile marine organisms. Sponges were by far the most abundant organism found on the pipes in terms of tissue volume. Other colonists included colonial

Figure 1: Diagram showing species of ascidians, spiny oysters, polychaete worms, and algae on sponge recruits among two sites in Belize (Blue Ground Range and Hidden the mangrove prop roots. On the 16 reef recruitment Creek). piles, sponges were also most abundant. Coral recruits, gorgonians, and algae made up some of the other sessile organisms. The recruitment piles in the Blue Ground Reef, however, experienced an influx of sediment in 2011, which may have smothered some of the individuals on those piles. A total of 20 sponge species were identified on the recruitment piles in the Blue

Ground Range, Belize and 13 species were identified on recruitment pipes in Hidden Creek,

Belize (Figure 1). Throughout this study, no species overlapped between these two sites.

However, not all species were identified for this study and those recruits were given designations such as species A, B, and C or were put into a group called “Other Sponges”. This may be affecting the total of species found within one or both of the habitats. Recruitment data for a total of 17 pipes and 16 recruitment piles, for Hidden Creek and the Blue Ground Range respectively, were added together for an average representation of species in terms of volume and number of individuals for each year. For Hidden Creek, the total volume found on the recruitment pipes increased every year, while the numbers of individuals stayed almost the same.

In 2009 a total of 124 individuals contributed a total volume of 2217 cm3, in 2010 a total of 124 9 individuals contributed a total volume of 2428 cm3, and in 2011 123 individuals contributed a total volume of 7861 cm3 (Figure 2c-d). In 2009 Biemna caribea (B. caribea) was the most abundant species by volume, contributing 37% of the total volume. In 2010 and 2011 Tedania ignis (T. ignis) was the most abundant species by volume, contributing 42% and 44% respectively of the total sponge volume (Figure 2c). The number of T. ignis individuals were lowest in 2011, (only contributing 4 individuals) but contributed by far the most volume out of all the sponge species. On the other hand, in 2011 B. caribea contributed 34 individuals, but only contributed 13% of the total volume that year. Many species had so little volume per individual that even with high individual numbers, they contributed very little to the total volume of their community. For example, Clathria campecheae had 60 individuals but contributed only 0.01% to the total volume over all three years (Figure 2d).

For the Blue Ground Range, the total volume of sponges found on the recruitment pipes was variable over 3 years, while the number of individuals decreased every year. In 2009 a total of 75 individuals contributed a total volume of 590 cm3, in 2010 a total of 59 individuals contributed 165 cm3, and in 2011 a total of 18 individuals contributed a total volume of 329 cm3

(figure 2a-b). In 2009 and 2011 Lissodendoryx colombiensis (L. colombiensis) contributed 36% and 50% of the total volume respectively for those years. Interestingly, in 2010 it only contributed 10% of the total volume (Figure 2a). L. colombiensis did not have significantly more recruits on the recruitment piles than other species found. For example, in 2009 Calyx podatypa had 6 individuals and contributed 10% of the total volume for that year while L. colombiensis had the same number of individuals but contributed 36% of the total volume.

Figure 2a Figure 2b

Figure 2c Figure 2d

Figure 2: Community dynamics for sponges on reef sites in Blue Ground Range, Belize and mangrove sites in Hidden Creek, Belize. The relative abundance of species is represented by total numbers of individuals and total volume. 11

Long Term Growth of Caribbean Reef Sponges

Figure 3 represents the net volume change of four Caribbean reef sponge species. The values used to measure the change in volume represent the magnitude at which the sponge grew from its original size. Net volume change at the end of 57 months ranged from 0.11 by

Verongula rigida (V. rigida) to 8.61 by Ircinia strobilina (I. strobilina). I. strobilina and

Iotrochota birotulata (I. birotulata) both generally had consistent increases (to 8.61 and 2.11 respectively) in net volume change over the 57 months (Figure 3b & 3d). V. rigida showed an increase of 0.72 at 32 months but decreased to 0.11 at the end of the experiment (Figure 3a), and

Ircinia sp. A showed an increase of 0.98 at 45 months but decreased to 0.63 at 57 months (Figure

3c). Figure 4 represents mean net volume change of the four Caribbean sponge species overlaid.

Figure 5 shows net volume changes measured over 57 months for all individuals of four species of Caribbean reef sponge on the Blue Ground Range.

Figure 3a Figure 3b

Ircinia sp. A Ircinia strobilina 3 14 2.5 12 2 10 1.5 8 1 6 0.5 4

0 2

Net ChangeVolume Net ChangeVolume -0.5 0 20 40 60 80 0 -1 -2 0 20 40 60 80 Time (Months) Time (Months)

Figure 3c Figure 3d

Figure 3: Net volume changes measured over 57 months for four species of Caribbean reef sponge on the Blue Ground Range: Verongula rigida, Ircinia sp. A, Iotrochota birotulata, and Ircinia strobilina. Sample sizes were 4-6 for each species. Sizes expressed as a proportion of initial volume. Note that the Y-axis ranges from maxima 0.8 to 10.

Specific Growth Rate Comparison 10

2 Net ChangeVolume 0 0 10 20 30 40 50 60 Time (Months)

Figure 4

Figure 4: Mean net volume change of the four Caribbean sponge species overlaid. Sizes expressed as a proportion of initial volume. Each line represents one species. Colors correspond with species colors and standard error bars

Ircinia sp. A Iotrochota birotulata 4 7 6 3 5 2 4 3 1 2

1 Relative Relative volume 0 Relative Volume 0 10 20 30 40 50 60 0 -1 -1 0 10 20 30 40 50 60 Time (Months) Time (Months)

Figure 5a Figure 5b

Ircinia strobilina Verongula rigida 20 2

15 1.5

10 1

5 0.5 Relative Relative Volume 0 Relative Volume 0 0 10 20 30 40 50 60 0 10 20 30 40 50 60 -5 -0.5 Time (Months) Time (Months)

Figure 5c Figure 5d

Figure 5: Net volume changes measured over 57 months for all individuals of four species of Caribbean reef sponge on the Blue Ground Range: Verongula rigida, Ircinia sp. A, Iotrochota birotulata, and Ircinia strobilina. Each line represents the growth of one individual. Sizes expressed as a proportion of initial volume. Note that the Y-axis ranges from maxima 2 to 18.

Discussion:

With no species overlapping between sites, the communities of sponges on the Blue Ground

Range and Hidden Creek recruitment substrata are shown to be different in species composition.

After three years, the Hidden Creek recruitment pipes became locally dominated in volume by

Tedania ignis (T. ignis), but the species showed intermediate levels of recruitment. The species abundance is also similar to that shown in Wulff’s (2009) study on the community dynamics of

Caribbean mangrove sponges. The study also showed that in a mature prop root community, T. ignis contributed 49% to 57% of the total volume of censused roots. It also shows that

Lissodendoryx isodictyalis (L. isodictyalis), Halichondria magniconulosa (H. magniconulosa),

Spongia spp, and Haliclona manglaris (H. manglaris) are relatively abundant in terms of the number of individuals in the mature prop roots as well, but not in terms of volume. The study mentions the striking disparity between the number of individuals and total volume of some of the sponge species. H. manglaris contributed 15.2% of the total sponge individuals found while only contributing 0.06% of the total volume. This trend was also noticed in this 2009-2011 study.

In 2011 H. manglaris contributed 12% of the total sponge individuals found and contributed

0.06% of the total sponge volume on the recruitment pipes. However, not all species followed previous studies’ trends. Specifically, Biemna caribea (B. caribea) and H. manglaris trended upwards in recruits over 3 years. These species have been shown to be efficient at colonization of bare mangrove roots but will be lost over time due to their low ability to persist on the root

(Wulff 2009). The findings in this study do not follow that trend.

This different trend in terms of the number of individuals from this 2009 to 2011 study may be indicative of the community still not quite at maturity. For example, Wulff's (2004) study 16 in Hidden Creek concluded that 20 months was insufficient for a mature prop root community to occur. In that study, 11 species were identified. In this study 13 species were identified over 3 years. Comparing this to Wulff’s (2009) study of sponge mature community dynamics on prop roots in the same mangrove habitat, a total of 19 species were identified. This difference in total species identified may be because of the different community maturity levels each of the studies ended on. Another hypothesis is that Wulff’s (2009) study had a larger sample size and different substrata with 24 roots initially being studied, whereas this study used 17 pipes. The species number in this study may be lower as well because some unidentified individuals were not able to be analyzed in time to include in this study and may have been a species not previously identified.

The Blue Ground Range was more variable in recruitment rate than Hidden Creek, with many species fluctuating in terms of the number of recruits and relative volume. These differences in species diversity may be explained in a few ways. Strong evidence shows that sponge species from mangrove ecosystems may be excluded from reef ecosystems by spongivores such as angelfish (Wulff 2005). Sponge species from reefs may be excluded from mangroves by being outcompeted by typical mangrove sponges (Wulff 1997). After 3 years, the number of individuals found on the Hidden Creek recruitment pipes went from 124 to 123, and the number of individuals found on the Blue Ground Range recruitment piles went from 75 to

18. As the communities became more established, it seems that the individuals' number stayed relatively the same in Hidden Creek, while falling in the Blue Ground Range. This discrepancy could be explained by the relatively low picoplankton levels on coral reefs (Wulff 2017) inhibiting the growth and success of sponges after settling. 17

To put the difference in recruitment communities of the Blue Ground Range and Hidden

Creek into perspective, understanding what the established community composition of both areas is vital. As mentioned earlier, a study by Wulff (2009) followed established communities in

Hidden Creek, finding a total of 19 species. In a study done by Wulff (2013), a total of 54 reef species were identified in the Blue Ground Range. The lower species diversity found in this study could indicate highly variable recruitment rates between species. There is lower diversity of species found in Hidden Creek, and this may be caused primarily by competitive exclusion by sponges as well as abiotic factors such as episodic salinity and temperature changes (Wulff

2004). In the Hidden Creek community, a relatively few numbers of species, such as T. ignis, B. caribea, and 7 other species made up 89% of the total biomass found. Due to the reef community not being driven primarily by competition between sponges, this may be why the Blue Ground

Range allows for higher species diversity. The difference in species found in the Blue Ground

Range between Wulff’s (2013) study and this study could be explained by the missing identification of some sponge individuals as mentioned before.

The variability in volume changes of the four reef sponge species may portray the characteristic responses each species has because of a combination of genotypic and environmental factors. By focusing on individuals of species through time series growth measurements, the data may show species characteristics that community-level studies may miss.

Overall, all species studied had positive growth at the end of the 57 months. Wulff’s (2013) study of recovery after extreme mortality followed populations of sponge species on the Blue

Ground range from 2006 to 2013 and found that the overall volumes of all sponges on the reef had dropped by 74%, yet we see positive growth in this study’s four species. This could be explained by the populations being in flux. Ircinia felix, a sponge species in the same genus as 18

Ircinia strobilina (I. strobilina) and Ircinia sp. A, showed high rates of regeneration rates after mortality events, but overall dropped significantly in total volume over Wulff’s 7 year study.

This implies that these positive changes in volume found may be a temporary upward trend and will ultimately drop in the future. I. strobilina’s massive-tough morphology (Wulff 2006c) may contribute to its growth rate because it does not have the propensity to fragment during disturbances and therefore lose volume. This species also had the highest accumulation of volume of all the species measured in this study. Their high regenerative efficiency and chemical defenses (Hoppe 1988) may also minimize loss and support consistent growth. On the other hand, V. rigida also falls under this morphology category, yet drops in volume from 32 months to 57 months. In Wulff’s (2013) study, when massive-tough sponges were hit by debris, they sometimes developed necrotic patches that spread over time. Damage to some or all of individuals of V. rigida at 32 months could account for the loss in volume. Iotrochota birotulata

(I. birotulata) consistently increased throughout all 57 months, yet it is considered an erect branching (Wulff 2006c) sponge. In Wulff’s (1991) study of asexual fragmentation, genotype success, and population dynamics of erect branching sponges, no individuals decreased in size during any time interval, and the species growth was shown to have a linear relationship to time.

The long-term growth data shows a similar trend and therefore may agree with previously found growth trends. Another erect branching species, Desmapsamma anchorata, showed rapid regeneration after partial mortality in its population, regenerating almost all of its mass in the year after a mortality event (Wulff 2013). This species shows just how variable growth can be in this environment. Ircinia sp. A’s modest drop in its volume may be explained by its growth morphology. It is a considered a massive-growth sponge, but due to its relatively large basal 19 attachment compared to other massive sponges (Wulff 2013), it may have been damaged and only suffered partial mortality, preventing a greater loss.

By looking at the total volume over all years and community differences between coral reef and mangrove sites in Belize, it is seen that trends in recruitment rate, species composition, and community dynamics are different between reefs in the Blue Ground Range and the mangrove prop roots in Hidden Creek. This may be because the different sponge species are highly adapted to their environments’ specific ecological and abiotic factors. In other studies, competition, predation, and food availability have been shown to influence sponges in these two habitats. From what was found in this study, these trends could be a likely explanation to the differences seen between sites. When measuring the growth rates of four of the most common species of Caribbean reef sponge, very different growth rates were observed between species.

The variability of community dynamics and growth of sponges deserves to be further studied, as these interactions give insight into how sponges support two distinct coastal marine ecosystems.

Acknowledgements:

I would like to thank my advisor Dr. Janie Wulff for providing guidance, Patience, and continue support throughout this project. Thank you to Dr. Kranz and Dr. Rassweiler for their guidance and feedback. Your attention and time is so greatly appreciated, and without the help of all committee members, I and this thesis would be lost. I would like to thank Bobbie Renfro,

Kate Hill, and Isabelle Badsen for their mentorship and advice on this project. Finally, thank you to my friends and family who supported me emotionally throughout this journey.

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