Research Article |
Corresponding author: James T. Fumo ( jfumo@hawaii.edu ) Academic editor: Tammy B. Robinson-Smythe
© 2024 James T. Fumo, Brian S. Powell, Randall K. Kosaki, Alison R. Sherwood.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Fumo JT, Powell BS, Kosaki RK, Sherwood AR (2024) Modeling the dispersal of the cryptogenic alga Chondria tumulosa (Rhodophyta, Ceramiales) in the Papahānaumokuākea Marine National Monument. Aquatic Invasions 19(3): 259-273. https://doi.org/10.3391/ai.2024.19.3.135377
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The cryptogenic nuisance alga Chondria tumulosa was first observed in 2016 at Manawai (Pearl and Hermes Atoll) in the Papahānaumokuākea Marine National Monument. It has since spread across the atoll, growing in thick mats and smothering benthic habitat. In September 2021 the species was observed at Kuaihelani (Midway Atoll), ~130 km to the northwest. Due to its growth habit and recent spread, considerable concern has been raised and management of the species may be warranted. We used publicly available oceanographic data and the Connectivity Modeling System software to assess how the potential for successful dispersal of C. tumulosa is affected by particle properties and oceanographic conditions. We found the likelihood of successful transit to be linked to particle density, oceanographic conditions at the time of release, and release location. Further modeling explicitly targeted the capacity of both reproductive tetraspores as well as drifting fragments to disperse. Model results indicated tetraspores of C. tumulosa are unlikely to survive the transit from Manawai to Kuaihelani, as none arrived at Kuaihelani above the depth limit of the species and those arriving below successfully settled at a rate of only 0.02%. In contrast, fragments modeled as rafting on marine flotsam such as macroalgae and marine debris settled at a rate of 3.85%. Rafting fragments also settled ~600 km further to the southeast (towards the Main Hawaiian Islands) than tetraspores. This study identified oceanographic conditions and particle properties likely to aid dispersal of C. tumulosa to Kuaihelani and suggests that fragments rafting on marine flotsam may accelerate its spread.
flotsam, Hawai‘i, marine debris, marine protected areas, phycology, rafting, tetraspores
The red alga Chondria tumulosa A.R.Sherwood & Huisman, 2020 was first observed in 2016 at Manawai in the Papahānaumokuākea Marine National Monument (PMNM) (
The main mechanism of expansion for C. tumulosa across Manawai appears to be vegetative fragmentation based both on field observations and genetic diversity information (
The Hawaiian archipelago lies in the North Pacific Subtropical Gyre with the islands themselves complicating flow (
The recent spread of C. tumulosa, the lack of macroalgal comparative examples, and the challenges in holistically assessing connectivity necessitates modeling techniques as a meaningful addition to our integrated understanding of dispersal in the species. The Connectivity Modeling System (CMS) is an individual-based biophysical stochastic lagrangian dispersal simulator (
Global HYCOM (
CMS simulated the release of 100 particles at each 3-hour interval, resulting in a cumulative total of 1,168,900 releases over the duration of the study period. Random release points were sampled from a region centered over Manawai with a latitudinal range of 27.740°N to 27.970°N and longitudes from 176.000°W to 175.700°W. Random particle release locations were selected at 0.001 degree intervals with replacement. Depths were sampled from 1–19 m at 0.1 m intervals with replacement. Release depth, latitude, and longitude were generated in R (
General model | Tetraspores only | Fragments only | |
---|---|---|---|
Release number | 1,168,900 | 116,890 | 116,890 |
Release rate | 100 particles per time step | 10 particles per time step | 10 particles per time step |
Particle size | 120 µm–5 m | 120–185 µm | 1 cm–5 m |
Particle density | 850–1150 kg/m3 | 1060–1150 kg/m3 | 850–1010 kg/m3 |
Release latitude | 27.740–27.970°N | 27.740–27.970°N | 27.740–27.970°N |
Release longitude | 176.000–175.700°W | 176.000–175.700°W | 176.000–175.700°W |
Release depth | 1–19 m | 1–19 m | 1–19 m |
Settlement polygons | 25 m depth contour | 25 m depth contour | 25 m depth contour |
Horizontal diffusivity | 2.5 m/s2 | 2.5 m/s2 | 2.5 m/s2 |
Vertical diffusivity | 0.5 m/s2 | 0.5 m/s2 | 0.5 m/s2 |
Time step | 10800 s | 10800 s | 10800 s |
A Generalized Additive Model (GAM) was implemented in R using the mgcv package to determine the impact of relevant variables on settlement success (
Further CMS modeling runs focused more specifically on tetraspore and fragment dispersal in order to compare the number of successful settlements directly under an equal number of releases in each case. Modifications to the parameters used for the general CMS model were necessary. Tetraspore density was restricted to 1060–1150 kg/m3 (
Of the 1,168,900 particles released from Manawai in the general model, 23,989 (2.05%) successfully settled at Kuaihelani. Settlement success of a particle at Kuaihelani was functionally linked to its density (p < 0.0001), the direction and strength of the currents at the time of release (p < 0.0001), and the location of release (p < 0.0001), according to the implemented GAM (Suppl. material
Generalized Additive Model (GAM) summary plots showing the zero-centered model predictions (ZCMP) for significant smooth terms. In panel (A) lower density is linked to higher settlement probability. Interactive effects of related terms as a contour are displayed for current velocity and direction (B) and release location (C). Dashed vertical lines in panel B represent the cardinal directions (N, E, S, W) and the solid vertical line represents the direct heading from Manawai to Kuaihelani (283 degrees). The black outline in panel (C) represents the 19 m depth contour of Manawai. The ZCMP are represented by the y-axis in (A) and by the color scale bars in (B, C).
Targeted model runs revealed that tetraspores released from Manawai successfully settled at Kuaihelani at a lower rate (0.02%) than rafting fragments (3.85%). None of the successful tetraspores (n = 29) settling at Kuaihelani did so within the observed depth range of the species. The percentage of tetraspores sinking below 100 m and 19 m after 5 days was 64.5% and 99.9%, respectively. Drift duration of successfully settling tetraspores ranged from 8.3 to 40.4 days. The same number of rafting fragments released from Manawai (n = 116,890) yielded 4,495 successful landings (Fig.
Total number of successfully settled particles released from Manawai. Islands are represented as blue dots with tetraspores shown above in black and fragments below in gray. Arrow width and associated numbers correspond to the number of successful settlements from Manawai to the settlement location of interest. The red box in the inset map in the top right corner shows the location of the study region with respect to the remainder of the Hawaiian Archipelago.
Overall, the particles most likely to successfully settle at Kuaihelani from Manawai are those with a density of less than 1010 kg/m3 released from the north-central portion of the atoll while swift northwest-bound currents occur over the release area. Particles with low densities drift for extended periods along the surface of the ocean while dense particles sink rapidly out of the modeled region. An apparent peak in dispersal likelihood at a density of ~1010 kg/m3 may be related to an avoidance of surface entrapment while sinking slowly enough to avoid export from the modeled region and a corresponding improvement in along-wind and cross-wind dispersion (
Tetraspores exist in a narrow range of physical properties in comparison to the range of particles included in the general model. While the particles are putatively negatively buoyant, with a density range of 1060–1150 kg/m³ (
The detectability of the species beyond the current depth limit may be constrained due to the cryptic nature of C. tumulosa in specific locations, the challenges posed by the remote nature of the islands, and the ongoing uncertainty regarding the abiotic or biotic factors influencing the depth limit of the species. Thus the depth at which tetraspores can survive may not be constrained to 19 m, increasing their likelihood of surviving transit to Kuaihelani.
Fragments were modeled identically to tetraspores with the exception of particle diameter and density, which were chosen to include a range of flotsam objects such as rafting mats, other macroalgae and marine debris, as these objects may aid in dispersal of marine organisms (
In both the tetraspore and fragment model runs, landings occurred beyond Kuaihelani with the two mechanisms exhibiting substantial divergences in maximum colonized distance. Fragments reached as far south as ‘Ōnūnui/ ‘Ōnūiki, ~600 km further than Kapou, the maximum extent of modeled tetraspore landings. The channel between Manawai and Kapou is considered a strong break point for the dispersal of marine organisms in the Hawaiian Archipelago and is reflected in both studies on oceanographic connectivity and population genetics (
While unable to unequivocally explain the dispersal of C. tumulosa in the PMNM, modeling provides a useful, timely, and economically feasible addition to our holistic understanding of this species of growing concern. Management actions suggested by these findings include the continuation of marine debris removal efforts especially in the north-central portion of Manawai, directing future aquatic invasive species monitoring surveys and eDNA work towards potential landing destinations, namely the windward (northeastern) sides of the atolls between and including Kapou and ‘Ōnūnui/‘Ōnūiki, and rigorously testing the dispersal potential of both native and invasive macroalgae, especially C. tumulosa. Although other algal outbreaks have been observed in PMNM these have been short lived and are not considered to have been invasive (
All authors conceptualized the research, assisted in study design and methodology, interpreted results, and reviewed and edited the manuscript. J.T.F. conducted the investigation, data collection, data analysis, and wrote the original draft.
This work was supported by grants secured by A.R.S. from the U.S. National Science Foundation (DEB-1754117) and the U.S. National Fish & Wildlife Foundation (NFWF 0810.20.068602).
The datasets generated and analyzed in the current study, along with the R scripts and statistical model outputs, are included in the supplementary material of this paper. For further inquiries or additional data requests, please contact the corresponding author.
We wish to thank one anonymous reviewer and Dr. Tammy Robinson whose feedback greatly improved the quality of this manuscript. We also with to thank Dr. Celia Smith, Dr. Brian Bowen, Dr. Feresa Cabrera, Kazumi Allsopp, Taylor Williams, Dr. Heather Spalding, Dr. Stacy Kreuger-Hadfield, and Keolohilani Lopes Jr. for providing helpful feedback and rewarding discussions during the writing of this manuscript.
Summary data frame
Data type: txt
Explanation note: Summary data frame in .csv format consisting of the release and settlement locations, particle properties, drift duration and distance, and oceanographic conditions at the time of release constructed from the raw CMS model output information.
R script implemented using S1 to produce S3
Data type: R file
Raw output statistics from the summary(), concurvity(), and gam.check() functions in R on the Generalized Additive Model (GAM) implemented in R using the mgcv package
Data type: docx
Raw connectivity output file resulting from a targeted CMS run releasing tetraspores from Manawai
Data type: cms
Raw connectivity output file resulting from a targeted CMS run releasing rafting fragments from Manawai
Data type: cms