The non-indigenous bryozoan, Amathia verticillata, has a worldwide distribution and commonly colonizes anthropogenic structures such as docks. Although widely recognized to house marine invertebrates within its structure, little is known regarding how the biogenic material produced by A. verticillata influences the marine community dynamics. The purpose of this study was to document the temporal patterns of A. verticillata and their associated marine invertebrate community in an urbanized estuary, Mission Bay, San Diego, CA, USA. We quantified A. verticillata percent cover and the abiotic conditions between July 2021–2022. The percent cover of A. verticillata varied temporally with temperature, with highest percent cover on docksides when temperatures were warmest. We also collected A. verticillata colonies of varying morphology and size to determine if abundance, density, and diversity of the marine invertebrate community associated with A. verticillata was influenced by its biogenic material and structural complexity. All invertebrates were identified to the lowest taxonomic level possible. We identified 20 families, 19 genera, and 12 organisms to species, representing 2 non-indigenous species (NIS), 2 likely NIS, 3 cryptogenic, and 5 native species. The most abundant taxonomic groups were marine amphipods, isopods, tanaids, and polychaetes. Furthermore, we identified juvenile stages and females with eggs living within A. verticillata. The invertebrate community varied significantly by A. verticillata morphotype and structural complexity. In general, there was greater invertebrate diversity in the elongated versus compact morphotype, and the invertebrate counts and diversity increased with structural complexity. Collectively, our results suggest that A. verticillata functions as a habitat-producing ecosystem engineer that may be providing an important nursery habitat for diverse groups of marine invertebrates, including other NIS, on anthropogenic structures.

Ecosystem engineers, structural complexity, non-indigenous species, nursery habitat, habitat-producing bryozoans

Non-indigenous species (NIS) are a pervasive problem in marine ecosystems (Vitousek et al. 1997; Chan and Briski 2017), driving ecological changes and threatening global biodiversity (reviewed in Bax et al. 2003). NIS are often characterized by rapid growth, and their establishment can affect resource availability for other organisms, and lead to declines in native species (Molnar et al. 2008; Katsanevakis et al. 2014; Geburzi and McCarthy 2018). Furthermore, some NIS act as ecosystem engineers that physically alter habitats by changing biotic or abiotic conditions (Jones et al. 1994; Jones et al. 1997). The effects of non-indigenous ecosystem engineers on community abundance and diversity can be variable (Guy‐Haim et al. 2017), and context-dependent (Crooks 2002). For instance, if non-indigenous ecosystem engineers become established on a homogeneous surface and increase complexity by producing multidimensional biogenic habitat, the associated community often increases in abundance, richness, and diversity (reviewed by Crooks 2002). One such non-indigenous structure-producing ecosystem engineer is the ctenostome bryozoan, Amathia verticillata (previously Zoobotryon verticillatum [Delle Chiaje, 1822]), also known as spaghetti bryozoan.

Amathia verticillata is found in relatively shallow, tropical to temperate areas (Cohen et al. 2005; Galil and Gevili 2014; Obaza and Williams 2018), where it grows densely, sometimes exceeding 1.5 m in length with branching, tangled noodle-like strands (McCann et al. 2015). It has a worldwide distribution; however, there is no universal agreement on its origin (Winston 1995; Galil and Gevili 2014; Marchini et al. 2015; Nascimento et al. 2021). Some suggest that A. verticillata is cryptogenic with an unknown native range (Nascimento et al. 2021), while others provide evidence for a Caribbean origin (Winston 1995; Galil and Gevili 2014), or indicate that this species is native to the Atlantic Ocean (Ounifi-Ben Amor et al. 2016). Despite this uncertainty, A. verticillata is commonly recognized as a NIS in the northeastern Atlantic (Amat and Tempera 2009), Mediterranean Sea (Ramadan et al. 2006; Galil and Gevili 2014), southern Mexican Pacific (Humara-Gil and Cruz-Gómez 2019), Galápagos Islands (McCann et al. 2015), Madeira Island (Wirtz and Canning-Clode 2009), Brazilian waters (Miranda et al. 2018), southeast coast of India (Jebakumar et al. 2017), and southern California (Cohen et al. 2005; Obaza and Williams 2018; Zavacki et al. 2024).

Amathia verticillata generally colonizes hard anthropogenic structures such as docks (Cohen and Carlton 1995; Winston 1995; Amat and Tempera 2009; Wirtz and Canning-Clode 2009; Obaza and Williams 2018), consequently providing a complex biogenic habitat on surfaces that might otherwise have a lower ecological value (Schlaepfer et al. 2011; Katsanevakis et al. 2014). Coupled with the observation that percent cover of A. verticillata often exceeds that of native species on anthropogenic substrates (Obaza and Williams 2018), A. verticillata has the potential to substantially impact the ecology of fouling communities on docks, especially for small benthic invertebrates that can play crucial roles in connecting trophic levels and influencing the function of ecosystems (e.g., Martins and Barros 2022; Ritter and Bourne 2024). Examples of the fauna associated with A. verticillata include mobile crustaceans such as amphipods (Guerra-García et al. 2011; Marchini et al. 2015; Guerra-García et al. 2024; Zavacki et al. 2024) and isopods (Marchini et al. 2015; Marchini et al. 2018; Guerra-García et al. 2024; Zavacki et al. 2024), polychaetes, pycnogonids, and bivalves (Farrapeira 2011; Guerra-García et al. 2024; Zavacki et al. 2024). Additional invertebrate and fish species also use drifting A. verticillata patches as ephemeral estuarine habitats (Pederson and Peterson 2002; Anderson et al. 2022).

In a recent study conducted along the Iberian Peninsula and north African coast, peracarid crustaceans, especially amphipods, dominated the macrofaunal communities associated with A. verticillata collected from docks within marinas (Guerra-García et al. 2024). Amphipods utilize microhabitats created by foundation species, and the trophic pathways they support contribute to ecosystem functioning (reviewed by Ritter and Bourne 2024). For example, amphipod grazing can determine the composition of fouling community assemblages by preventing periphyton and ascidians from colonizing and overgrowing seagrasses (Duffy and Harvilicz 2001). Thus, the fouling community dynamics along docks colonized by A. verticillata could be driven by the macrofauna that reside within A. verticillata. To begin to understand the ecological role of the amphipods and other invertebrates that inhabit A. verticillata, a critical first step is identifying which species are present and their relative abundances. We also need to identify the invertebrate community to determine whether A. verticillata facilitates the establishment and spread of other NIS as has been shown along the Iberian Peninsula and north Africa where seven NIS accounted for more than 50% of the total abundance of the macrofaunal species collected in A. verticillata (Guerra-García et al. 2024). There is concern that if A. verticillata facilitates the establishment of other NIS, there could be negative synergistic impacts on native species, resulting in an invasion meltdown (Guerra-García et al. 2024).

Mission Bay, San Diego, CA, USA is an urbanized estuary where A. verticillata is known to colonize docks (Dexter and Crooks 2000; Tracy and Reyns 2014; Obaza and Williams 2018; Zavacki et al. 2024). While the presence of A. verticillata in Mission Bay has been previously documented, in this study we systematically characterized the temporal dynamics of A. verticillata colonization with respect to the environmental conditions at one site in Mission Bay and identified the associated invertebrate community to determine the degree to which A. verticillata serves as a habitat for other NIS. Furthermore, we examined if abundance, density, and diversity of the marine invertebrate community associated with A. verticillata was influenced by the biogenic material produced by, and structural complexity of, A. verticillata. To date, the role that the A. verticillata biogenic structure itself plays in determining the community dynamics of its inhabitants is not well understood.

The first goal of our study was to document the temporal patterns of A. verticillata colonization to understand how A. verticillata and its associated invertebrate community changed over time. Elsewhere (see Zavacki et al. 2024) we document the spatial patterns of A. verticillata colonization in Mission Bay. Here, we focused our efforts at one site, the South Shores (32°45.85'N, 177°13.05'W) dock in Mission Bay, San Diego, California, USA (Fig. 1), because A. verticillata has been consistently observed here during the last decade (Reyns, personal observation), and sampling at one site allowed for sampling on a relatively high-resolution temporal scale (usually weekly, but see below) from July 2021 to July 2022. To examine the environmental conditions that might impact the colonization of A. verticillata, a YSI ProDSS (digital sampling system) handheld multiparameter meter was used to record a point measure of surface temperature, salinity, and dissolved oxygen (DO). Precipitation data was also collected at the San Diego Airport (Menne et al. 2012), located ~9.65 km from the center of Mission Bay. To determine how the distribution of A. verticillata varied weekly, we quantified the percent cover of A. verticillata on the dock within 5 randomly selected 25 × 25 cm fixed quadrats. These data were used to calculate the average percent cover of A. verticillata per week.

Figure 1. 

Map of Mission Bay, San Diego, CA with sampling station, South Shores denoted by the star. Inset shows location of San Diego in California, USA for reference.

To identify the invertebrate community associated with A. verticillata, three replicate colonies (of low, medium, and high biogenic material; see below for definitions) were collected from locations on the dock outside of the fixed quadrats, once per week from July through December 2021, when colonies disappeared. Collections were resumed once per month after colonies returned to the dock, from March through June 2022 (n = 84 samples). Upon collection, each A. verticillata colony was categorized by morphotype (compact: ≤ 25 cm or elongated: > 25 cm from the dock). Amathia verticillata and their associated marine organisms were collected by surrounding the colony (depending on its size) with a 100 µm, 18 × 42 cm or 10.5 × 20 cm mesh bag, placing the sample into a gallon-sized Ziplock bag, and storing it in a cooler with ice to prevent degradation during transport to the lab for further processing.

In the laboratory, each A. verticillata colony was removed from the collection bags and placed in a 5-gallon bucket filled with seawater. The A. verticillata colony was shaken 10 times by hand to remove all associated marine organisms, and the colony was returned to the Ziplock bag for processing after sample sieving. The bucket water was filtered through nested 100, 200, and 400 µm mesh sieves to collect the organisms associated with A. verticillata. This process was repeated three times to ensure that most of the organisms had been successfully removed from each A. verticillata colony (as determined by a pilot study: Zavacki 2023). Organisms were placed in containers by sieve size and preserved in 100% ethanol until they could be counted and identified.

Each A. verticillata colony was removed from its Ziplock bag and five random kenozooids per colony were selected to measure widths using a Meiji Techno stereo microscope with a RZ PLAN 1× lens and an ocular micrometer. Once measured, the colony was placed in a drying oven at 50 °C for 24 h to obtain the A. verticillata dry weight of each sample. The preserved invertebrate samples were divided using a Folsom plankton splitter if they were dense, then sorted under a Meiji Techno stereo microscope with a RZ PLAN 1× lens. Organisms were separated into broad taxonomic groups: amphipods, isopods, tanaids, polychaetes, copepods, unknowns, and other organisms that could be identified but were less abundant, such as gastropods, bivalves, and nematodes (called “others”). The organisms collected in the 100 µm sieve were primarily pelagic copepods which were assumed to be swimming in and around A. verticillata colonies and not necessarily using the bryozoan as a benthic habitat; thus, they were not identified to species and were excluded from further analysis. The 200 and 400 µm sieved amphipods, isopods, tanaids, and polychaetes were identified to the lowest taxonomic level possible using published resources (SCAMIT 2004; Fofonoff et al. 2018; SCAMIT 2023) and by working with taxonomists (Dean Pasko and Tony Phillips, personal communication). Species names and systematic arrangement of taxa were arranged following the World Register of Marine Species (WoRMS Editorial Board 2023). In addition, invertebrates were categorized into four main life history stages: immature organisms, adults (males and females without eggs), females with eggs, and unknowns. Finally, we classified the introduction status for the 12 peracarid crustaceans and polychaetes that we could identify to species as native, NIS, likely NIS, and cryptogenic using published records (Menzies 1952; Chapman 2007; Maloney 2007b, a; Fofonoff et al. 2018) and taxonomic experts (Dean Pasko and Tony Phillips, personal communication). The ‘likely NIS’ category were species of uncertainty because their biogeographic ranges prevented their inclusion in the other defined categories.

Given that the size of A. verticillata colonies varied by collection, we standardized the invertebrate counts within A. verticillata by dividing the number of organisms collected per colony by the dry weight of that colony. Thus, we used density (number of invertebrates per gram of dry weight of A. verticillata) as the response variable to compare the marine invertebrate communities associated with each A. verticillata morphotype (compact versus elongated). To determine if the amount of A. verticillata biogenic material, or structure, influenced the associated invertebrate community, we also separated the weekly A. verticillata samples into three bins based on the A. verticillata dry weight: low, defined as < 0.5 g (n = 44 replicates), medium defined as 0.5–5 g (n = 28 replicates), and high defined as > 5 g (n = 12 replicates). We considered these A. verticillata dry weight bins, which are a way to quantify the amount of biogenic material in each colony, to serve as a proxy for structural complexity based on observations that colonies that were larger and greater in weight, were also bushier and more developed with branching stolons. All invertebrates were counted and identified to the lowest taxonomic level possible as described above. We used the raw counts (not standardized by A. verticillata dry weight) to compare the marine invertebrate communities by structural complexity bin.

When we started sampling in July 2021, the percent cover of A. verticillata colonies was ~20% but increased to over 80% less than one month later (Fig. 2A). During the peak of A. verticillata coverage, we observed colonies that extended from the dock to the sediment below (~2.6 m deep) as well as small patches that covered the benthos adjacent to the dock. Percent cover was above 20% through the fall months, before declining in October 2021, and disappearing from the dock sides from January 4 through March 15, 2022 (Fig. 2A). In the spring, A. verticillata percent cover increased from 0% in March to 7.6% in July 2022 when sampling was terminated. This seasonal pattern in A. verticillata percent cover followed the seasonal temperature patterns we observed (Fig. 2A). Although there were temperature fluctuations throughout the sampling period, temperatures decreased overall during the fall months from a 25.8 °C high in August to the 14.2 °C low in late December 2021 and increased through the spring months. Additionally, during the period of relatively low A. verticillata percent cover, there were periodic decreases in salinity (e.g., late October 2021, late December 2021, and early April 2022) that corresponded to rain events; indeed, the lowest salinities corresponded to the late fall through early spring months when precipitation occurred (Fig. 2B). While salinity fluctuated weekly, it generally remained between 33–34 PSU throughout the study period. Similarly, DO varied weekly, but values were above 4 mg L^-1 throughout the study period (Fig. 2C). Generally, DO values were highest during the winter through early spring months when temperatures were the lowest (Fig. 2A, C). Overall, when we examined the relationship between the percent cover of A. verticillata and the abiotic conditions, there was a significant positive relationship between A. verticillata and temperature (Spearman correlation coefficient = 0.74, p < 0.0001). There were also significant relationships between temperature and salinity (Spearman correlation coefficient = 0.51, p < 0.0004) as well as temperature and DO (Spearman correlation coefficient = -0.87, p < 0.0001), whereby increasing temperatures corresponded to increasing salinity and decreasing DO. Given the autocorrelations between abiotic variables, we did not run additional correlations between the percent cover of A. verticillata and salinity or DO.

Figure 2. 

Amathia verticillata percent cover and abiotic conditions. (A) Amathia verticillata percent cover (left y-axis) and temperature (right y-axis), (B) salinity (left y-axis) and precipitation (right y-axis), and (C) dissolved oxygen (DO) over time.

Within A. verticillata, we identified marine invertebrates from 20 families, 19 genera, and 12 species (Table 1). Of the invertebrates we could identify to species, we observed more native species (e.g., Paracerceis sculpta and Odontosyllis phosphorea) than introduced species (e.g., Aoroides secunda and Paranthura japonica) at the beginning of sampling until A. verticillata experienced a winter die-off (Figs 2A, 3). Interestingly, once A. verticillata started to grow back on the dock in March 2022, the first species to recolonize were NIS, along with possibly less common species, given the relatively high percentage (e.g., > 80%) of unknown species also observed during this time (Table 1, Fig. 3). Native species returned to the A. verticillata after the introduced species and appeared to increase in relative abundance as A. verticillata became more established (Fig. 3). An important consideration is that during most sampling dates, more than half the of the organisms we collected were immature juveniles that could not be identified to species.

Figure 3. 

Introduction status and % composition of the invertebrate community associated with Amathia verticillata over time. Introduction status from top to bottom are % of species in Amathia verticillata that were: cryptogenic (black), likely NIS (yellow), NIS (grey), native (orange), and unknown (blue) during the sampling times (once per week from July - December 2021, and once per month from March - June 2022; noted as Month/Day/Year).

The most abundant taxonomic groups we identified inhabiting A. verticillata were amphipods, isopods, tanaids, and polychaetes (Fig. 4A). Amphipods dominated our samples, but the relative abundance of each taxonomic group varied slightly by A. verticillata morphotype, with more amphipods, isopods and tanaids collected in compact A. verticillata than in the elongated morphotype (Fig. 4A). In contrast, the elongated morphotype had more polychaetes (33.4% composition) than in the compact morphotype (only 7.3%; Fig. 4A). In both morphotypes, tanaids made up less than 1% of the community composition (Fig. 4A). Notably, both A. verticillata morphotypes housed all life history stages of these invertebrate groups with immature organisms being the most frequently observed in the compact (67.1%) and elongated (49.1%) morphotypes (Fig. 4B). There were slightly more adult stages in the compact (18.5%) than elongated (15.5%) morphotype, and relatively small percentages of reproductive females (2.3–5%; Fig. 4B). However, a number of individuals collected could not be identified, and the elongated morphotype had more than three times the percent of unknown species (i.e., immature stages) in comparison to the compact morphotype (Fig. 4B).

Figure 4. 

Amathia verticillata morphotype and invertebrate composition. Composition of taxonomic groups (top row) and life history stages (bottom row) of peracarid crustaceans and polychaetes associated with Amathia verticillata compact (left columns) and elongated (right columns) morphotypes. Percentages by: (A) invertebrate groups: amphipods, tanaids, isopods, and polychaetes, and (B) life history stages: immature (juveniles), females with eggs, adults (males and females without eggs), and unknowns.

Overall, there were differences between the A. verticillata morphotypes and their associated marine invertebrate communities. A t-test indicated that there was a significant difference between kenozooid width of the two morphotypes (t₁₀₉ = -2.634, p = 0.01), with elongated kenozooids having significantly greater widths than those of the compact morphotype. Furthermore, the marine invertebrate community varied significantly by morphotype (PERMANOVA, F_1,79 = 2.45, p = 0.02, 9956 unique permutations). The average invertebrate densities were similar in compact and elongated colonies (Fig. 5A), but invertebrate diversity was slightly higher in elongated colonies (H’: 1.94 ± 0.05) than in compact colonies (H’: 1.61 ± 0.06; Fig. 5B). There were also slight differences in the percent contribution of families to the invertebrate communities associated with the compact and elongated morphotypes (Table 2). Compact colonies had an average similarity of 58.08%, whereas the elongated colonies had an average similarity of 65.91% (Table 2). The highest contributions to the similarities in the invertebrate community were > 13% and by the same isopod family (Sphaeromatidae; Table 2) for both morphotypes. Additionally, the Corophiidae amphipods had a higher percent contribution to the communities in the compact than elongated morphotypes (15.83% versus 9.58%, respectively; Table 2). The Podoceridae amphipods also had a higher percent contribution to the communities in the compact than elongated morphotypes (13.69% versus 11.02%, respectively; Table 2). In contrast, the Hyalidae, Ampithoidae and Amphilochidae amphipods, and Syllidae polychaetes had higher percent contributions in the elongated colonies than the compact colonies (Table 2). The average dissimilarity between the two morphotypes was 39.25% (Table 2). Although the Hyalidae amphipods were the highest contributing invertebrate family to those differences, all invertebrate family contributions to the differences were under 8% (Table 2).

Figure 5. 

Amathia verticillata morphotype and invertebrate density and diversity. Average ± standard error of the peracarid crustaceans and polychaete invertebrate (A) density (# individuals/dry weight of Amathia verticillata) and (B) diversity (represented by the Shannon-Wiener Diversity index, H’), associated with Amathia verticillata compact and elongated morphotypes.

With respect to A. verticillata structure, the marine invertebrate community varied significantly by structural complexity bin (PERMANOVA, F_2,81 = 13.3, p = 0.0001, 9919 unique permutations). Average invertebrate count increased with increasing A. verticillata structural complexity from ~147 individuals in low structural complexity, ~726 individuals in the medium structural complexity, and ~2,195 individuals in the high structural complexity bin (Fig. 6A). Likewise, invertebrate diversity also increased from the low (H’: 1.49 ± 0.07) to medium (H’: 1.92 ± 0.05) structural complexity bins but was relatively similar between medium and high structural complexity (H’~1.9; Fig. 6B). The SIMPER analysis indicated that the average similarity among the bins was above 52%, with increasing similarity as A. verticillata structural complexity increased (Table 3). Sphaeromatidae isopods were the greatest contributor to these similarities, ranging ~ 12–19% contribution among each A. verticillata structural complexity bin (Table 3). The Corophiidae and Podoceridae amphipods had relatively high percent contributions to the community when A. verticillata had low structural complexity, with decreasing percent contributions as structural complexity increased (Table 3). In contrast, the Hyalidae amphipods had relatively high contributions to the communities when A. verticillata had medium to high structural complexity (Table 3). The low and high A. verticillata structural complexity bins had the greatest average dissimilarity (54.66%; Table 3). The invertebrate families all contributed less than 10% to these differences between A. verticillata structural complexity bins (Table 3).

Figure 6. 

Amathia verticillata structural complexity and invertebrate density and diversity. Average ± standard error of the peracarid crustaceans and polychaete invertebrate (A) counts, and (B) diversity (represented by the Shannon-Wiener Diversity index, H’), associated with Amathia verticillata structural complexity bins, low: < 0.5 g, medium: 0.5–5 g, and high: > 5 g.

In Mission Bay, we observed seasonal changes in the percent cover of A. verticillata, which broadly followed observed temperature fluctuations. Amathia verticillata dominated the sides of the dock at the end of the summer/early fall with greater than 80% cover, but as has been reported elsewhere (Winston 1995; Coleman 1999; Micael et al. 2018; Guerra-García et al. 2024), colonies declined once temperatures decreased below 19 °C (October). Indeed, experiments indicate that growth and sexual reproduction of A. verticillata are limited by temperature (Bullivant 1968). In the winter (between December and February), A. verticillata disappeared from the sides of the dock, similar to observations from the Indian River Lagoon, Florida where A. verticillata died-back when the first cold fronts lowered water temperatures (Winston 1995). In addition to the quadrats we sampled on the dock sides, video surveys taken on the undersides documented the absence of A. verticillata on all floating dock surfaces during the winter in Mission Bay (Zavacki, personal observation). The ability of A. verticillata to recolonize docks relatively quickly as temperatures increased in the spring suggests that a source of new individuals might exist locally. Winston (1995) hypothesized that A. verticillata fragments overwinter to produce new growth the next spring. This might also be true in Mission Bay if the benthos acts as a repository for A. verticillata fragments that can resume sexual reproduction and release larvae in the spring. Alternatively, when a colony undergoes fragmentation, pieces of stolon may form resting buds that can eventually re-attach to substrates and grow into a new colony (as discussed in Geiger and Zimmer 2002). It is unknown whether resting buds remained attached to the dock surfaces but were too small to be readily observed, or whether such buds can reside in the sediment below the docks and become resuspended during storms or by boats to foster recolonization when environmental conditions become optimal for growth.

The period with the lowest A. verticillata percent cover (fall through early spring months) and temperatures corresponded to increased rain events, more variable salinity, and slightly higher DO as storms occurred. Such events were often accompanied by increased winds, and coupled with the lower temperatures, may have led to more detachment from the docks and fragmentation of A. verticillata. Together with tidal flushing, these environmental conditions may prevent A. verticillata from accumulating under the docks and causing local decreases in DO when A. verticillata degrades. During this study, DO at South Shores did not fall below levels considered stressful for biological activity (< 2–3 mg/L; https://www.epa.gov/ms-htf/hypoxia-101). Overall, salinity in Mission Bay throughout the year was within the optimal salinity range (22–35 PSU) documented for A. verticillata (Nair et al. 1992). Thus, it is unlikely that the survival of A. verticillata was hindered by the salinity in Mission Bay.

While benthic, calcifying bryozoans provide complex habitats for diverse assemblages of infaunal organisms (reviewed in Wood et al. 2012; Wood and Probert 2013), non-calcifying species such as A. verticillata that are commonly found in fouling communities on anthropogenic structures similarly house a variety of marine invertebrates (Winston 1995; Pederson and Peterson 2002; Guerra-García et al. 2011; Minchin 2012; Marchini et al. 2015; Dailianis et al. 2016; Marchini et al. 2018; Guerra-García et al. 2024). In this study, we identified 20 families representing peracarid crustaceans (amphipods, isopods, and tanaids) and polychaetes that were associated with A. verticillata. While the species we observed differed at times to those observed in other studies, there were commonalities among the families represented in A. verticillata, including the Caprellidae, Sphaeromatidae, and Paranthuridae (Guerra-García et al. 2011; Marchini et al. 2015; Marchini et al. 2018; Guerra-García et al. 2024), suggesting that A. verticillata supports similar assemblages of organisms across its global distribution.

At South Shores, we identified five native species, two NIS, two likely NIS, and three cryptogenic species. If we eliminate the organisms we could not identify (e.g., the “unknowns”), unlike Guerra-García et al. (2024), we observed higher abundances of native species within A. verticillata compared to the cryptogenic and NIS, for most weeks. This was particularly true at the beginning of our study when A. verticillata was already established on the docks in Mission Bay. Interestingly, once A. verticillata returned to the dock in March 2022, the first organisms to recolonize were also NIS. This could imply that introduced species are among the early colonizers of A. verticillata. However, it is important to note that differences in sampling approaches (e.g., using fine-meshed nets to capture the A. verticillata community in this study verses hand collections in Guerra-García et al. 2024) may have led to the preponderance of immature stages that we observed in our samples, but could not identify to species to determine introduction status. Since many early developmental stages have subtle or difficult morphological differences to distinguish, one next step would be to incorporate molecular tools to identify these immature organisms, which would better resolve whether the relative abundance of the invertebrates using A. verticillata in Mission Bay are NIS or native species. As such, we do not know the degree to which invader-invader mutualism occurs at our study area. Furthermore, experimental studies that focus on the recruitment processes and interactions between native and NIS in A. verticillata are imperative for understanding the community dynamics among these species.

Most studies have identified and described fauna collected within A. verticillata without quantifying or standardizing by the amount of biogenic material collected (e.g.,Winston 1995; Farrapeira 2011; Minchin 2012; Ferrario et al. 2014; Marchini et al. 2015; Dailianis et al. 2016; Marchini et al. 2018), or by using A. verticillata volume (Anderson et al. 2022; Guerra-García et al. 2024) rather than dry weight to standardize collections as used herein. Given this variability in sampling techniques, it is challenging to make comparisons across studies of the overall densities of marine invertebrates found in A. verticillata. Of the more detailed studies that have reported densities of infauna associated within bryozoans, an average of 35.9 individuals of the amphipod Caprella scaura Templeton, 1836 were collected per gram of the bryozoan Bugula neritina Linnaeus, 1758 (Guerra-García et al. 2011), and mean values ranged between 22.1–83.4 total organisms g^-1 of dry weight of A. verticillata (Pederson and Peterson 2002). However, in this study we collected 1–2 orders of magnitude greater abundances of marine invertebrates within A. verticillata than previously reported (Pederson and Peterson 2002; Guerra-García et al. 2011). Previous studies with A. verticillata either collected the colonies with other species (Anderson et al. 2022) by scraping the dock (Ferrario et al. 2014; Dailianis et al. 2016), or by hand (Pederson and Peterson 2002; Marchini et al. 2015; Marchini et al. 2018; Guerra-García et al. 2024). These methodologies potentially characterize different assemblages than those in our study, with some potential loss of highly mobile species, and as described above, the immature stages. Our approach of collecting A. verticillata colonies with fine-meshed bags may have served to capture more of these small, mobile crustaceans, and likely explain why invertebrate densities within A. verticillata were so high in Mission Bay.

We observed two morphotypes (compact and elongated) of A. verticillata in Mission Bay, and as reviewed in Marchini et al. (2015). It is unclear if these morphotypes represent two different species of A. verticillata, but a recent study (Nascimento et al. 2021) supports the claim that there is only one species of A. verticillata found worldwide. There was a difference between the kenozooid width of the two morphotypes with significantly greater width of kenozooids in the elongated colonies. Elongated colonies may reach 2 m in length (Minchin 2012), and the thicker kenozooids might provide more structural support to minimize fragmentation, as bigger colonies become more vulnerable (Micael et al. 2018). It is unlikely that kenozooid width directly impacted the invertebrate community, but we observed some differences in the associated marine invertebrates based on the morphological characteristics of A. verticillata. In terms of taxonomic groups, the elongated A. verticillata colonies had more polychaetes, whereas the compact A. verticillata colonies had more tanaids, isopods, and amphipods. Polychaetes may readily use the elongated A. verticillata morphotype as a habitat if the more open configuration provides a better shelter for these organisms. In contrast, the higher abundance of amphipods in the compact A. verticillata colonies could result from the variety of microhabitats provided by the typically higher number of branches and nodes found in the compact colonies in comparison to the elongated morphotype. Similarly, when the algae Sargassum spp. had higher numbers of branches and hydroid coverage, there was a positive correlation with amphipod richness, density, diversity, and evenness (Carvalho et al. 2018; Carvalho et al. 2022). Alternatively, the amphipods that are abundant in the compact morphotype could be outcompeting the polychaetes and reducing their abundances. Therefore, more studies are needed to examine and better understand the ecological interactions between the organisms that are using A. verticillata as a habitat.

Overall, the invertebrate communities in the two A. verticillata morphotypes were relatively similar as the same invertebrate families were found in each morphotype. For example, the isopod Sphaeromatidae family contributed the highest to the invertebrate community in both morphotypes. This likely reflects the relatively high isopod abundances observed in this region of Mission Bay (Zavacki et al. 2024). Furthermore, Paracerceis sculpta (Holmes 1904), the main species found in the Sphaeromatidae family in our study, is distributed worldwide in warm-temperate to tropical harbors, and is considered a NIS in many areas (Fofonoff et al. 2018). Paracerceis sculpta was found within A. verticillata in the Azores Archipelago of Portugal (Marchini et al. 2018), and select locations of southeast Atlantic shelf, Alboran Sea, and west mediterranean (Guerra-García et al. 2024). This species is also associated with a variety of other organisms, including sponges, found underneath rocks, and among algae (Fofonoff et al. 2018; Stebbins and Wetzer 2023), suggesting that this is an opportunist species when it comes to finding a habitat (Stebbins and Wetzer 2023).

However, other species may choose A. verticillata morphotypes as a result of multiple complex interactions, such as a behavioral choice, refuge from physical stresses, predation and/or competition, as well as a place for mating or feeding (reviewed in Stachowicz 2001). In addition, species sometimes respond to local structural complexity rather than to the overall patch size of habitat (e.g., Taniguchi et al. 2003). Perhaps, the smaller localized structures of the elongated A. verticillata colonies provide greater refuge from predators, shelter from hydrodynamic flow, and contain more resources (Fenwick 1976; Heck and Wetstone 1977; Hacker and Steneck 1990; Russo 1990) than the overall structure of the compact A. verticillata colonies. This may also help explain why invertebrate diversity was slightly higher in elongated than compact A. verticillata colonies.

An important consideration is that the amount of biogenic material produced by A. verticillata might have a larger effect on the invertebrate community dynamics than the arrangement of the material (compact or elongated). For example, a previous study with the shrimp Palaemon macrodactylus Rathbun, 1902 determined that the total amount of material, and not how it was arranged, was the primary factor that determined the shrimp’s habitat (Crooks et al. 2016). Our observations that invertebrate counts and diversity increased with A. verticillata structural complexity are aligned with the results from other studies indicating that structural complexity increases species diversity (Stoner and Lewis 1985; Crooks 2002; Graham and Nash 2013; Darling et al. 2017). Additionally, the similar invertebrate diversity in the medium and high complexity bins, suggests that the amount of A. verticillata material predominately benefited the invertebrate community diversity when the A. verticillata dry weight was greater than 0.5 g.

The invertebrate communities varied significantly with A. verticillata structural complexity (low, medium and high); however, the highest average similarity was among the most structurally complex bin (i.e., > 5 g) where the community may have been well-established. The invertebrate contributions were mainly driven by the same families, but their percent contribution to the community varied based on the A. verticillata structural complexity. In addition, as structural complexity increased, the invertebrate community contribution became more even, without any one family dominating the community. Again, the Sphaeromatidae isopods were the greatest contributor to the invertebrate community regardless of the structural complexity. The second highest contributor was from families Corophiidae, Podoceridae, and Hyalidae for the low, medium, and high structural complexity bins, respectively, and included species identified as cryptogenic or likely NIS to Mission Bay (Chapman 2007; Maloney 2007b, a; Fofonoff et al. 2018).

In general, the structure of A. verticillata colonies had marked influence on their associated peracarid crustacean and polychaete communities. These taxa appear to be especially responsive to the effects of invasive, structure-producing ecosystem engineers, including a mussel (Arcuatula (=Musculista) senhousia W. H. Benson, 1842) that creates dense byssal mats in Mission Bay (Crooks 1998), a tube-building polychaete worm Ficopomatus enigmaticus Fauvel, 1923 that creates reefs in Mar Chiquita Lagoon, Argentina (Schwindt and Iribarne 2000), and invasive seaweeds in the Gulf of Maine (Dijkstra et al. 2017). As highlighted above, many mechanisms are potentially operating simultaneously to drive the patterns of increased diversity and densities often seen within biogenically complex habitats (McCoy and Bell 1991; Crooks 2002), and it can be difficult to tease them apart (Matias et al. 2007; Crooks et al. 2016). For A. verticillata in Mission Bay, however, it appears that facilitative effects go beyond simply attracting and aggregating individuals, as indicated by the presence of juveniles and females with eggs (Fig. 4). It has been suggested that invasive engineers might serve as nursery habitat for resident biota (e.g., Wallentinus and Nyberg 2007; Bruschetti 2019), and in aquatic systems, examples include crabs in F. enigmaticus reefs (Luppi and Bas 2002), shrimp in beds of the freshwater algae Myriophyllum spicatum (Alford and Rozas 2019), and sea slugs in turfs of the algae Vaucheria sp. on tidal flats (Reise et al. 2023). Indeed, juveniles and reproductive females of C. scaura were also collected in A. verticillata along the eastern Atlantic coast (Guerra-García et al. 2011), suggesting that A. verticillata serves as a nursery habitat for other NIS. Because of the demographic implications of invaders increasing the fitness of resident organisms (whether they be native or non-native species), this topic merits further descriptive and experimental attention. Furthermore, the colonization of A. verticillata on floating structures such as docks is increasing the availability of structurally-complex habitats near the surface in Mission Bay, rather than along the bottom (such as those typically provided by eelgrass). This might be shifting the distribution of the peracarid crustaceans using A. verticillata from benthic habitats to floating anthropogenic structures. Thus, the relatively high abundance of amphipods in A. verticillata may result in alterations to the local trophic dynamics and benthic-pelagic coupling (e.g., Ritter and Bourne 2024) in areas with many docks. Once we characterize the species utilizing A. verticillata habitats, we should focus on developing experimental approaches to improve understanding the ecological interactions among these species and the possible broader ecosystem implications of their presence.

Given the rapid growth and extensive structure created by A. verticillata, it is often considered a nuisance biofouler where it has invaded (e.g., Pestana et al. 2020; Guerra-García et al. 2024). By their nature, ecosystem engineers typically have multi-faceted and cascading effects within ecosystems (Crooks 2002), and further comprehensive studies across a range of systems should be undertaken to better characterize the role of A. verticillata and inform management strategies associated with this NIS.

We identified an abundant and diverse marine invertebrate community associated with the habitat-forming non-indigenous bryozoan, A. verticillata in Mission Bay, California. The invertebrate community was primarily composed of peracarid crustaceans and polychaetes, with a mix of native, cryptogenic, and NIS. Thus, more work should be conducted to determine if A. verticillata disproportionately supports native or non-native species. We also observed juveniles and reproductive female life history stages living within A. verticillata, suggesting that these organisms are using A. verticillata as a nursery habitat. While A. verticillata morphology influenced the associated marine invertebrate community, the amount of biogenic material produced by A. verticillata significantly increased the abundance of organisms within A. verticillata, as well as the invertebrate community diversity. Overall, the results from this study suggest that A. verticillata is an ecosystem engineer that provides structurally complex habitat on anthropogenic substrates for many marine invertebrates, and increases invertebrate community density, abundance, and diversity.

EMZ: research conceptualization, sample design and methodology, investigation and data collection, data analysis and interpretation, original draft: writing - review & editing. NBR: research conceptualization, sample design and methodology, data analysis and interpretation, second draft: writing - review & editing. JAC: research conceptualization, sample design and methodology, interpretation, and final draft: writing - review & editing. MAB: research conceptualization, sample design and methodology, interpretation, and final draft: writing - review & editing.

The authors received funding from the University of San Diego, from a Faculty Research Grant to NBR for support of field sampling supplies and the Stephen W. Sullivan/Sister Dale Brown Memorial Marine Science Scholarship to EMZ to attend PRIMER and PERMANOVA workshops. Publication was made possible by a grant from the College of Arts and Sciences, University of San Diego. Additionally, EMZ was awarded a travel award to attend the International Conference of Marine Bioinvasions (ICMB) conference.

Scientific Collecting Permit, General Use (ID: GM-200090002-20009-001) to the Department of Environmental and Ocean Sciences.

We are extremely grateful to Dean Pasko and Tony Phillips of Dancing Coyote Environmental in San Diego County, CA for their assistance in identifying the associated marine community. We would like to thank Marti Anderson and Adam Smith for their assistance in using the PRIMER-e v.7 and PERMANOVA statistical software. We appreciate the two anonymous reviewers who helped improve this manuscript with their insightful comments. We would also like to thank the University of San Diego undergraduates who helped with the field collections and sample processing in the lab: Kelly Hayden, Sivanna Trainer, Sara Timney, Katherine (Kate) Hoffman, Kyra Allison, Katherine (Katie) Power, Laila Richards, Julia Humphrey, Sienna Doering, Sam Stelter, Ella Crotty, Gina Choi, Paul Cleary, Maria Angst, Kaylee McCoy, Kai Monteil-Doucette, and Madeleine (Maddie) Glenna.