# Seabird nutrient subsidy alters size and resource use of functionally important mangrove macroinvertebrates

Jennifer Appoo, Nicholas a J Graham, Christopher W Jones, Sébastien Jaquemet, Nancy Bunbury

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## To cite this version:

Jennifer Appoo, Nicholas a J Graham, Christopher W Jones, Sébastien Jaquemet, Nancy Bunbury. Seabird nutrient subsidy alters size and resource use of functionally important mangrove macroinvertebrates. Ecosphere, 2024, 15 (12), pp.e70121. 10.1002/ecs2.70121. hal-05483010

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# Seabird nutrient subsidy alters size and resource use of functionally important mangrove macroinvertebrates

Jennifer Appoo<fnref n="1" />,<fnref n="2" />

<figure><img src="image_3.png" /></figure>

Nicholas A. J. Graham<fnref n="3" />

Christopher W. Jones<fnref n="2" />

Sébastien Jaquemet<fnref n="1" />

Nancy Bunbury<fnref n="2" />,<fnref n="4" />

**Correspondence**

Jennifer Appoo UMR ENTROPIE, Université de La Réunion, Saint Denis, La Réunion, France

Email: jennifer.appoo@univ-reunion.fr

**Present address**

Jennifer Appoo, Blue Economy Research Institute, University of Seychelles, Anse Royale, Mahé, Seychelles.

**Funding information**

Bertarelli Foundation, Marine Science Programme; African World Heritage Fund, Moses Mapesa Research Grant; La Région Réunion, Doctoral Fellowship; PADI Foundation, Marine Research Grant

**Handling Editor:** Sunshine A. Van Bael

**Abstract**

Invertebrates have a central role in food webs and ecosystem functioning. By boosting productivity, allochthonous nutrient inputs influence the food webs of recipient communities. Understanding how allochthonous nutrient subsidies affect invertebrates is crucial, particularly in highly productive coastal areas. Here, we examine how mangrove macroinvertebrates are impacted by nutrient-rich guano delivered by nesting seabird populations at Aldabra Atoll in the Indian Ocean. We compare nitrogen and carbon stable isotope ratios and nitrogen composition of basal resources and macroinvertebrate consumers in mangroves with and without nesting seabirds. Seabird-derived nutrient enrichment increased the nitrogen content of basal food sources and herbivorous littorinid gastropods and sesarmid crabs. In mangroves with breeding seabirds, mean carapace widths of sesarmid and omnivorous portunid crabs were 6% and 11% larger, respectively. Isotopic niches of littorinid gastropods and sesarmid crabs were larger and had higher overlap at seabird compared to non-seabird sites. Epiphytic macroalgae and guano comprised >50% of resource contributions to littorinid gastropods and sesarmid crabs at seabird sites. This differed markedly from non-seabird sites where the main resource contributions were 77% mangrove leaves for littorinid gastropods, 36% sediment organic matter, and 41% mangrove leaves for sesarmid crabs. The increased sizes of mangrove crabs suggest that seabird nutrient enrichment can promote mangrove crab fisheries productivity and benefit the provisioning of mangrove ecosystem services. By shifting resource use of functionally important macroinvertebrates, we discuss how seabirds modify trophic interactions, with potential consequences for mangrove ecosystem processes and resilience.

**KEYWORDS**

allochthonous nutrients, crabs, gastropods, isotopic niche, mangrove trophodynamics, resource contribution, Seychelles, stable isotopes

This is an open access article under the terms of the [Creative Commons Attribution License](https://creativecommons.org/licenses/by/4.0/), which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

© 2024 The Author(s). *Ecosphere* published by Wiley Periodicals LLC on behalf of The Ecological Society of America.

<figure><img src="image_4.png" /></figure>

<footnote n="1">¹UMR ENTROPIE, Université de La Réunion, Saint Denis, La Réunion, France</footnote>

<footnote n="2">²Seychelles Islands Foundation, Victoria, Mahé, Seychelles</footnote>

<footnote n="3">³Lancaster Environment Centre, Lancaster University, Lancaster, UK</footnote>

<footnote n="4">⁴Centre for Ecology and Conservation, University of Exeter, Penryn, Cornwall, UK</footnote>
# INTRODUCTION

The movement of nutrient resources across ecosystem boundaries considerably impacts the functioning and dynamics of recipient communities (Anderson & Polis, 2004). Natural allochthonous nutrient inputs increase primary and secondary productivity, with their influence propagating throughout food webs, generating a wide range of ecosystem responses (Polis et al., 1997; Sanchez-Pinero & Polis, 2000). Invertebrates are the most abundant and diversified animal group worldwide, comprising 80% of all known eukaryote species (Brusca & Brusca, 2003). They occupy a wide range of ecological niches, making them crucial components of food webs and fulfilling key functions vital for maintaining ecosystem integrity and delivering ecosystem services (Kotze et al., 2022; Wilson, 1987). For example, invertebrates influence primary production through seed dispersal, pollination, and herbivory and act as ecosystem engineers by forming and modifying habitats through bioturbation and bioerosion (Prather et al., 2013). Investigating how invertebrates respond to nutrient subsidies is important to gain insight into the impacts of allochthonous nutrient inputs on ecosystem functioning and service delivery.

Seabirds forage at sea and transfer marine nutrients to land at their breeding and roosting sites, mainly as guano deposits (Grant et al., 2022). Guano provides a natural nutrient subsidy for island and coastal ecosystems worldwide (De La Peña-Lastra, 2021) and indirectly boosts food webs around seabird colonies by enriching primary producers. Seabirds also provide direct nutrient subsidies in terrestrial systems through consumers that feed on seabird tissues, carcasses, eggs, or discarded marine prey (Kolb et al., 2011). Seabird nutrient subsidies influence the abundance, diversity, and behavior of terrestrial and aquatic invertebrate consumers (Kolb et al., 2011; Young et al., 2011). However, research to date has predominantly focused on temperate or polar regions. Many tropical communities are severely threatened by climate change and local stressors, and important questions remain about how tropical ecosystems will respond to biodiversity loss (Clarke et al., 2017). Tropical areas have higher environmental complexity and species diversity, which may result in different ecological responses to nutrient inputs. A global meta-analysis on the effects of seabird nutrient subsidies on invertebrates reveals that only 6% of studies have been conducted in tropical regions (Van Der Vegt & Bokhorst, 2023). This underrepresentation limits our ability to draw firm conclusions about global patterns of seabird effects (Grant et al., 2022) and to fully understand how seabird nutrient subsidies influence invertebrate communities in biodiversity-rich tropical coastal areas.

Mangroves, which can host huge nesting seabird colonies, are a crucially important coastal habitat, acting as carbon sinks, connecting land and sea habitats, providing nurseries for marine species, protecting tropical coastlines, and supporting the livelihoods of coastal communities (Worthington et al., 2020). Mangroves support unique and diverse invertebrate assemblages, particularly crustaceans and mollusks. These groups play major ecological roles in mangrove ecosystem functioning (Ferreira et al., 2024), including carbon and other nutrient cycling, sediment bioengineering (Cannicci et al., 2008), mangrove growth regulation (Lee, 2008), and act as food resources for numerous vertebrates (Nagelkerken et al., 2008; Sandoval et al., 2022). Nesting and roosting seabirds can contribute substantial quantities of nutrient-rich guano to mangrove forests (Irick et al., 2015; McFadden et al., 2016). Nutrient enrichment of mangrove habitats influences invertebrate community structure and trophic relationships (Feller & Chamberlain, 2007; Valiela et al., 2004). Onuf et al. (1977) showed that seabird-derived nutrients increased mangrove leaf nutritional quality, resulting in increases in biomass of folivorous insects and herbivory rates.

Similarly, fertilization experiments have shown that nutrient enrichment can lead to either increased or decreased consumption of mangroves, depending on the feeding guild and behavior of the herbivores (Feller, 1995; Feller et al., 2007; Feller & Chamberlain, 2007), suggesting that nutrient enrichment causes a shift in resource use. However, these studies solely focused on mangroves as a food source. In mangrove habitats, consumers can access various additional primary food sources, such as sediment organic matter (SOM), macroalgae, and benthic microalgae (BMI; Nagelkerken et al., 2008). The effects of nutrient enrichment on these various sources and the consequences on resource use in mangrove invertebrate food webs remain poorly explored. Furthermore, invertebrates occupy multiple trophic levels in mangroves, yet nutrient enrichment studies have investigated the effects mainly on primary consumers (Feller et al., 2013). Research in other coastal invertebrate food webs shows that nutrient subsidies are incorporated at multiple trophic levels (Silva et al., 2022), and nutrient enrichment increases consumer sizes (Hemmi & Jormalainen, 2002) and alters community trophic structure (Vizzini et al., 2016; Wimp et al., 2019). Whether this response is consistent for multilevel and functionally important mangrove invertebrate communities, such as gastropods and crabs, remains to be examined. Such investigations are essential to understanding the functioning of naturally subsidized mangrove ecosystems.

Here, we investigate how seabird nutrient subsidies impact the macroinvertebrate food web in the mangrove forests of Aldabra Atoll (Seychelles). Following previous
analyses confirming seabird nutrient enrichment of this
mangrove ecosystem (Appoo, Bunbury, et al., 2024), we
aim to assess the trophic response of the
macroinvertebrate community to seabird-derived nutri-
ents. We use stable isotopes of nitrogen (δ¹⁵N) and car-
bon (δ¹³C) and total nitrogen concentration (%N) of basal
food sources and macroinvertebrate consumers sampled
in mangroves with and without nesting seabirds. In food
webs, there is a stepwise increase in δ¹⁵N per trophic
level (Post, 2002), resulting in high δ¹⁵N values in
high-trophic level marine predators, like seabirds. After
guano deposition, volatilization of ammonia results in
further enrichment of δ¹⁵N in guano, causing elevated
δ¹⁵N values in seabird-subsidized systems
(Kazama, 2020). In contrast, δ¹³C values vary little
among trophic levels, closely reflecting values of organic
matter at the base of food webs (Post, 2002). Carbon
derived from marine sources exhibits higher δ¹³C than
terrestrial sources. Due to their coastal location, man-
grove communities can display δ¹³C gradients ranging
from terrestrial (depleted) to marine (enriched) values
(Bouillon et al., 2011). Therefore, δ¹⁵N and δ¹³C values
can demonstrate the functioning of ecosystems by show-
ing nutrient or energy flow in food webs, identifying the
sources of nutrients and organic matter assimilated by
consumers, and characterizing trophic niches and inter-
actions (Layman et al., 2012). Specifically, we aim to
determine whether seabird-derived nutrients increase the
nitrogen composition of mangrove food web components
at multiple trophic levels. At seabird sites, we expect the
availability of enriched food sources will lead to (1) larger
sizes of macroinvertebrate consumers and shifts in their
resource use, as indicated by (2) broader isotopic niches
and (3) higher contributions of enriched resources to con-
sumer diets, compared to non-seabird sites.

METHODS

Study area

Aldabra Atoll (9°24' S, 46°20' E), in the southern Seychelles, is a large raised coral atoll (total area 365 km²) in the Western Indian Ocean (Appendix S1: Figure S1). The atoll comprises four main islands (total land area 155 km²) surrounding a shallow lagoon. The atoll hosts 78% of the total mangrove area in Seychelles (~1700 ha; 11% of Aldabra's land area; Walton et al., 2019). Aldabra's mangroves occur along the lagoon shores and islets, with *Rhizophora mucronata* as the most dominant mangrove species, followed by *Ceriops tagal*, *Bruguiera gymnorrhiza*, and *Avicennia marina* (Macnae, 1971). The mangroves are influenced by semidiurnal tides ranging

from 2 to 3 m amplitude (Farrow & Brander, 1971). Aldabra has a semiarid climate with mean annual temperatures of 24-28°C, mean annual rainfall of 975 mm, and two distinct seasons (Haverkamp et al., 2017): the wet season during November-April influenced by the northwest monsoon winds, and the dry season during May-October influenced by the southeast trade winds.

Aldabra's mangroves host large nesting seabird populations in single and mixed-species colonies, comprising great frigatebirds *Fregata minor*, lesser frigatebirds *Fregata ariel*, and red-footed boobies *Sula sula* (Burger & Betts, 2001). Their distribution coincides with the absence of feral cats; there are fewer breeding seabirds on the largest island of Grande Terre, the only island with a feral cat population. Seabirds occur year-round in Aldabra's mangroves due to multiple breeding peaks, long breeding cycles, and roosting patterns of non-breeding individuals. Nesting frigatebirds and red-footed boobies contribute around 41.4 and 40.9 tonnes of nitrogen and phosphorus per year, respectively, to Aldabra's mangroves, enriching mangrove food webs (Appoo, Bunbury, et al., 2024). Human influence on the atoll is limited to the presence of a small research station with 10-20 permanent staff. Aldabra's remoteness and protection as a Strict Nature Reserve and UNESCO World Heritage Site have ensured that the mangroves and seabird colonies are relatively undisturbed.

Field sampling

Sampling occurred between November 2022 and March 2023 during the breeding period of all three seabird species. We collected samples at 10 sites distributed along the lagoon shores around the atoll, ensuring a minimum distance of 1 km between each site. We selected sites based on the breeding seabird distribution, with five sites with low (<20 nests) nesting activity and five sites with high nesting activity (250-700 nests; Appendix S1: Figure S1).

We sampled the main basal food sources in man-
groves (Nagelkerken et al., 2008), taking into account the
feeding behavior of the consumers (Phillips et al., 2014):
green mangrove leaves, epiphytic macroalgae, SOM, and
BMI (see below). At each site, samples of basal resources
were collected in eight random quadrats, each measuring
5 × 5 m and spaced at least 50 m apart along the man-
grove fringe (total site length 400 m). Within each quad-
rat, we collected between one and three samples of each
basal resource. R. mucronata comprise 79% of mangrove
trees at our surveyed sites (Appoo, Bunbury, et al., 2024),
making it the dominant mangrove food source. We col-
lected young, fully expanded green R. mucronata leaves
exposed to the sun. Six leaves were sampled from at least three individual trees and pooled to form one composite sample per quadrat. Epiphytic macroalgae (Chlorophyta) were collected randomly on *R. mucronata* roots using forceps. SOM was collected by inserting a PVC corer (diameter = 22 mm) into the top 2-cm sediment layer. Collection of BMI was not possible without SOM or other organic matter contamination; therefore, we used average stable isotope values compiled from mangroves in semi-arid and arid regions (see below).

We sampled three of the most abundant macro-invertebrate consumers in this system. Mangrove periwinkle snails of the genus *Littoraria* are ubiquitous in Aldabra's mangroves (Taylor, 1971) and are generalist herbivores, consuming mangrove tissues, fungi, microalgae and macroalgae, and lichen on mangroves (Alfaro, 2008; Christensen et al., 2001; Lee et al., 2001). Three *Littoraria* spp. individuals were collected randomly in each quadrat on mangrove trees from different substrates, including leaves, roots, and trunks. Sesarmid crabs, *Leptarma leptosoma*, are abundant on *R. mucronata* on Aldabra (Macnae, 1971), feeding primarily on green mangrove leaves but also consuming algae and sediment (Bouillon et al., 2002; Dahdouh-Guebas et al., 1999). We collected 15 individuals randomly on mangroves in each site. As a secondary consumer, we sampled the portunid omnivorous crab *Thalamita crenata* on intertidal mudflats adjacent to mangrove forests. *T. crenata* is a generalist predator and scavenger, consuming mainly macroinvertebrates such as mollusks and crustaceans but also algae and plant detritus (Cannicci et al., 1996; Dahdouh-Guebas et al., 1999). Adjacent to each site (<50 m from mangrove fringe), we sampled 7–10 *T. crenata* crabs, except for one seabird site where the crabs were absent. We collected a total of 987 samples of basal food sources (seabird sites n = 253 and non-seabird sites n = 258) and macro-invertebrate consumers (seabird sites n = 231 and non-seabird sites n = 245). Details of sample sizes for each site and sample type are provided in Appendix S1: Tables S1 and S2. Additionally, we collected guano from active nests of frigatebirds (n = 27) and red-footed boobies (n = 32) at seabird sites as the main source of seabird-derived nutrients. All samples were kept on ice during daytime field sampling until arrival at laboratory in the evening.

## Sample processing and isotope analysis

Plant samples were rinsed with fresh water. For each *Littoraria* spp. individual, we measured the shell height using calipers (±1 mm) and sampled their foot muscle. We measured crab carapace width using calipers (±1 mm)

and collected body muscle from sesarmid crabs and limb muscle from portunid crabs. All samples were dried in an oven at 60°C for at least 48 h. Samples were powdered using a ball mill, and subsamples were weighed and placed in tin capsules. δ¹⁵N and δ¹³C values were measured using an Isoprime 100 Isotope Ratio Mass Spectrometer with international standards IAEA-600, USGS-41, and IAEA-CH6, at the stable isotope facility at Lancaster University (Lancaster, UK). Epiphytic macroalgae and SOM samples were analyzed separately for δ¹³C and δ¹⁵N. Before δ¹³C analysis, dry subsamples were rinsed repeatedly with 10% v/v HCl to remove carbonates, washed with distilled water, and dried again. Results are expressed in delta notation in ppm (‰) following the equation:

$$ \delta^{13}\text{C} \text{ or } \delta^{15}\text{N} = \left( \frac{R \text{ sample}}{R \text{ standard}} \right) - 1, \quad (1) $$

where R = ¹³C/¹²C or ¹⁵N/¹⁴N, using Vienna Pee Dee Belemnite as the standard value for carbon and atmospheric nitrogen for nitrogen. Accuracy based on internal standards was within 0.1‰ SD for δ¹³C and 0.2‰ SD for δ¹⁵N. Selected samples were run in triplicate to ensure accuracy of readings further. Variations in tissue lipid content can influence δ¹³C values; therefore, we used mathematical normalization methods to standardize the lipid content of samples following Post et al. (2007). For basal plant samples, equations were applied according to carbon content (% C), while invertebrate samples were normalized if C:N ratios were >3.5. The equations used were as follows:

$$ \text{plants} < 40\% \text{C} : \delta^{13}\text{C}_{\text{normalized}} = \delta^{13}\text{C} - 3.02 + 0.09 \times \text{‰C}, \quad (2) $$

$$ \text{plants} > 40\% \text{C} : \delta^{13}\text{C}_{\text{normalized}} = \delta^{13}\text{C} - 5.84 + 0.14 \times \text{‰C}, \quad (3) $$

$$ \text{aquatic animals} : \delta^{13}\text{C}_{\text{normalized}} = \delta^{13}\text{C} - 3.32 + 0.99 \times \text{C} : \text{N}, \quad (4) $$

## Data analysis

### Isotopic and nitrogen composition of food web components

We produced a δ¹³C and δ¹⁵N biplot comprising all food web components at seabird and non-seabird sites. To verify whether δ¹⁵N enrichment through seabird nutrient subsidies resulted in a higher %N of food web components, we assessed the linear relationships between
$\delta^{15}$N and %N using Spearman rank correlations. We tested the influence of nesting seabird presence on $\delta^{13}$C using linear mixed models for each food web component using the “lmer” function from R package *lme4* (Bates et al., 2015). Models included seabird status as a fixed effect and site as a random effect. We performed diagnostics on model residuals to verify normality, homogeneity of variance, and independence using the “plot” function from the R package *car* (Fox & Weisberg, 2019).

## Consumer size

We tested the influence of seabird nutrient subsidies on consumer size by assessing the linear relationships between $\delta^{15}$N and consumer size using Spearman rank correlations. For each consumer, we then performed parametric or nonparametric *t* tests, as appropriate, to assess differences in consumer size between seabird and non-seabird sites.

## Consumer isotopic niche space

We compared consumer isotopic niches between seabird and non-seabird sites by plotting the isotopic niche space of each consumer and their standard ellipse areas based on maximum likelihood estimates. We computed ellipses containing 95% of the data (SEA) and 40% of the data corrected for small sample size (SEA~C~) and convex hulls using functions “createSiberObject” and “groupmetricsML” from R package *SIBER* (Jackson et al., 2011). We assessed the % niche overlap, measured as the proportion of overlap between standard ellipses of consumers. To account for uncertainty in the data, we also estimated the Bayesian standard ellipse areas (SEA~B~) for each consumer using Monte Carlo Simulation with $10^4$ iterations, using functions “siberMVN” and “siberEllipses.” We determined the probability that SEA~B~ posterior distributions are smaller (or larger) between seabird and non-seabird sites for each consumer.

## Resource contributions to consumer diet

We estimated the relative contribution of different resources to consumers at seabird and non-seabird sites using Bayesian stable isotope mixing models with R package *MixSIAR* (Stock & Semmens, 2016). For herbivorous littorinid gastropods and sesarmid crabs, we included BMI, mangrove leaves, epiphytic macroalgae, and SOM as potential food sources. For omnivorous portunid crabs, potential resources were BMI, mangrove

leaves, epiphytic macroalgae, littorinid gastropod, and sesarmid crabs. Guano can also be consumed directly and was included as a food source for consumers at seabird sites. We ran separate models for each consumer and status and applied mean $\delta^{15}$N and $\delta^{13}$C values (±SD) of each food source according to their seabird status. Aldabra is a semiarid oceanic atoll (Farrow, 1971); therefore, BMI stable isotope values applied were average for mangroves in arid and semiarid regions; $\delta^{13}$C = -15.7 ± 3.0‰ and $\delta^{15}$N = 2.0 ± 1.9‰ suggested by Medina-Contreras et al. (2023), compiled from various sources (Akbari Noghabi et al., 2022; Hsieh et al., 2002; Shahraki et al., 2014). Trophic enrichment factors (mean ± SD) used varied depending on the consumer. For littorinid gastropods, we applied $\delta^{13}$C = 5.3 ± 0.3‰, $\delta^{15}$N = 4.2 ± 0.2‰ (Teoh et al., 2018), and for sesarmid crabs, $\delta^{13}$C = 5.4 ± 0.9‰, $\delta^{15}$N = 3.9 ± 0.5‰ (Sandoval et al., 2022), from trophic discrimination experiments of gastropods and crabs feeding on mangroves, respectively. For portunid crabs, we used $\delta^{13}$C = 1.3 ± 0.3‰ commonly assumed by McCutchan et al. (2003) and $\delta^{15}$N = 3.4 ± 1.0‰ (Post, 2002) according to their high-protein diet (Le et al., 2017). Models were fitted using three chains and “very long” Markov chain Monte Carlo lengths using the function “run_model,” and convergence was checked based on the Gelman–Rubin and Geweke diagnosis using the function “output_JAGS.”

## RESULTS

### Isotopic and nitrogen composition of food web components

At seabird sites, littorinid gastropods had the highest $\delta^{15}$N values, while SOM had the lowest $\delta^{15}$N values. In contrast, at non-seabird sites, portunid crabs exhibited the highest values of $\delta^{15}$N and mangrove leaves had the lowest (Figure 1). At both seabird and non-seabird sites, portunid crabs were the most enriched in $\delta^{13}$C (most marine group), while mangrove leaves were the most depleted in $\delta^{13}$C (most terrestrial group).

%N increased with $\delta^{15}$N for all basal sources, with SOM and epiphytic macroalgae showing the highest increase (SOM: $r_s$ = 0.57, *p* < 0.0001, *n* = 239; epiphytic macroalgae: $r_s$ = 0.62, *p* < 0.0001, *n* = 192; mangrove leaves: $r_s$ = 0.44, *p* < 0.0001, *n* = 80; Figure 2a). We observed similar positive correlations between %N and $\delta^{15}$N for littorinid gastropods ($r_s$ = 0.36, *p* < 0.0001, *n* = 240) and sesarmid crabs ($r_s$ = 0.38, *p* < 0.0001, *n* = 150), but not for portunid crabs ($r_s$ = -0.09, *p* = 0.44, *n* = 86; Figure 2b). $\delta^{13}$C did not differ between seabird and non-seabird sites for all food web components (Appendix S1: Figure S2).
<figure><img src="image_5.png" /><figcaption>**FIGURE 1** Biplot of normalized δ¹³C and δ¹⁵N (means and 95% CIs) of seabird guano, basal sources, and consumers at seabird and non-seabird sites.</figcaption></figure>

## Consumer size

We found no correlation between δ¹⁵N and size (shell height) of littorinid gastropod ($r_s = -0.2, p = 0.76, n = 240$) and no difference in shell height between seabird and non-seabird sites ($W = 7575, p = 0.49$; Figure 3a,b). However, size (carapace width) increased with higher δ¹⁵N values for both sesarmid ($r_s = 0.38, p < 0.0001, n = 150$; Figure 3c) and portunid crabs ($r_s = 0.28, p = 0.01, n = 86$; Figure 3e). Sesarmid and portunid crabs were both larger at seabird than at non-seabird sites (respectively, $W = 3525, p = 0.007$; $t = 2.97, df = 83, p = 0.004$; Figure 3d,f).

## Consumer isotopic niche space

Niche overlap differed between seabird and non-seabird sites, mainly between littorinid gastropods and sesarmid crabs (Figure 4a,b). The proportion of overlap between their isotopic niches (indicated by $SE_{A_C}$ ellipses) was higher at seabird sites (28.1%) than at non-seabird sites (14.7%). Overlap in isotopic niches between littorinid gastropods and portunid crabs, as well as between sesarmid and portunid crabs, was only observed with their SEA ellipses (Figure 4a,b). The proportion of overlap between littorinid gastropods and portunid crabs was similar at seabird (12.9%) and non-seabird sites (13.0%). For sesarmid

and portunid crabs, overlap was slightly higher at seabird sites (20.3%) than at non-seabird sites (17.2%).

The isotopic niche width of littorinid gastropods and sesarmid crabs at seabird sites shifted upward along the δ¹⁵N axis compared to non-seabird sites (Appendix S1: Figure S3). For portunid crabs, the isotopic niche width at seabird sites contracted along the δ¹³C axis compared to non-seabird sites. Isotopic niche size, indicated by $SE_{A_B}$, of littorinid gastropods was larger (probability = 0.99) at seabird sites (median, 95% credibility intervals: 19.2‰, 16.0–2.9‰) than at non-seabird sites (14.3‰, 11.8–16.9‰; Figure 4c,d). Sesarmid crabs also had larger isotopic niches (probability = 0.92) at seabird sites (8.41‰, 6.55–10.3‰) than at non-seabird sites (6.61‰, 5.20–8.22‰). In contrast, the isotopic niche size of portunid crabs was smaller (probability = 0.99) at seabird sites (9.81‰, 6.88–13.4‰) than at non-seabird sites (16.3‰, 12.1–21.3‰).

## Resource contributions to consumer diet

There were marked differences in the relative contribution of food resources to consumers between seabird and non-seabird sites. For littorinid gastropods, the dominant food resources were epiphytic macroalgae (35%, 0.4%–61%) and guano (34%, 26%–44%) at seabird sites and mangrove leaves (77%, 64%–85%) and BMI (14%, 6.7%–22%)
<figure><img src="image_6.png" /><figcaption>**FIGURE 2** Linear relationships between %N and δ¹⁵N for (a) basal resources and (b) consumers. Points represent raw data, and shaded areas represent 95% CIs. All linear relationships were significant except for portunid crabs.</figcaption></figure>

at non-seabird sites (Figure 5a). For sesarmid crabs, the main food resources were epiphytic macroalgae (29%, 2.7%–58%) and guano (28%, 19%–40%) at seabird sites and mangrove leaves (41%, 20%–68%) and SOM (36%, 2.2%–72%) at non-seabird sites (Figure 5b). For portunid crabs, the main food resources were BMI and sesarmid crabs, comprising higher proportions at non-seabird sites (BMI: seabird = 38%, 29%–48%, non-seabird = 51%, 36%–73%; sesarmid crab: seabird = 20%, 0.8%–48%, non-seabird = 34%, 7.7%–53%; Figure 5c).

DISCUSSION

We show that seabird nutrient subsidies strongly influ-
ence mangrove macroinvertebrate trophic relationships.

Seabird-derived nutrient enrichment increased the nitro-
gen content of basal food sources and primary con-
sumers, as well as the sizes of herbivorous and
omnivorous crabs at seabird sites. In mangroves with
nesting seabirds, herbivorous gastropods and crabs
switched to enriched resources, leading to greater isoto-
pic niche sizes and niche overlap compared to mangroves
without nesting seabirds. Our results provide broad
insights into how seabird nutrient subsidies can influence
mangrove ecosystem processes and service delivery.

Nesting seabirds contribute substantial nitrogen to Aldabra's mangroves, enriching all food web components (Appoo, Bunbury, et al., 2024). The positive relationships between δ¹⁵N enrichment and %N confirmed that seabird subsidies enhance the nutrition of basal food sources. This effect was 1.5 times stronger in SOM and epiphytic
<figure><img src="image_7.png" /><figcaption>**FIGURE 3** Linear relationships between size of consumers and δ¹⁵N for (a) littorinid gastropods, (c) sesarmid crabs, and (e) portunid crabs. Shaded areas represent 95% CIs. Sizes of (b) littorinid gastropods, (d) sesarmid crabs, and (f) portunid crabs at seabird and non-seabird sites. Boxplots display median and interquartile range. Different letters denote significant (*p* < 0.05) differences between means. Solid and open circles represent raw data for seabirds and non-seabird sites, respectively.</figcaption></figure>

macroalgae than in mangrove leaves, probably because most seabird guano in mangroves is deposited directly onto the sediment at low tide or into the water at high tide, elevating seawater and sediment nutrient

concentrations (Appoo, Bunbury, et al., 2024). The higher nitrogen content in epiphytic macroalgae than in mangroves is likely due to their faster nutrient uptake from the water column (Hong et al., 2019).
<figure><img src="image_8.png" /><figcaption>**FIGURE 4** Isotopic niche space showing niche overlap between macroinvertebrate consumers at (a) seabird and (b) non-seabird sites. Solid and dashed lines represent standard ellipse areas containing 40% (SEA~C~) and 95% of the data (SEA), respectively. Isotopic niche sizes, represented by Bayesian standard ellipse areas (SEA~B~), of macroinvertebrate consumers at (c) seabird and (d) non-seabird sites. Violin plots show data distribution; boxplots display median and interquartile range.</figcaption></figure>

Elevated δ¹⁵N values also correlated with increased nitro-
gen in littorinid gastropods and sesarmid crabs but not
in portunid crabs. Seabird-derived nutrient enrichment is
usually highest for primary consumers compared to sec-
ondary consumers (Kolb et al., 2011). Similar results in
terrestrial invertebrates suggest that subsidy enrich-
ment of higher trophic levels may not be reflected in
tissues due to nutrient use for more complex

metabolic processes (Obrist et al., 2022). Littorinid gas-
tropods exhibited the highest δ¹⁵N values at seabird
sites, which can be due to sample contamination of
their foot muscle from passing through guano on man-
grove substrates. However, an increase in %N linked to
seabird-derived nutrient enrichment is plausible.
Similar effects have been documented in other mol-
lusks, such as the periwinkle *Littorina brevicula* and
<figure><img src="image_9.png" /><figcaption>**FIGURE 5** Isotope mixing model estimates of relative contributions of different resources to the diet of (a) littorinid gastropods, (b) sesarmid crabs, and (c) portunid crabs at seabird and non-seabird sites. Boxplots display median and interquartile range.</figcaption></figure>

mussel *Mytilus* spp. or *Septifer* sp. near seabird colonies on Rishiri Island (Kazama, 2020) and the common limpet *Patella vulgata* and acorn barnacle *Semibalanus balanoides* at seabird colonies on the Farne Islands (Healing et al., 2024). The absence of $\delta^{13}C$

differences between seabird and non-seabird sites indicates minimal influence of seabirds on organic matter inputs in mangrove food webs, consistent with findings from other terrestrial and coastal food webs (Choy et al., 2010; Gagnon et al., 2013).
Sesarmid and portunid crabs were approximately 6% and 11% larger, respectively, at seabird sites. Crab growth is facilitated by the assimilation of high-quality resources (Kristensen et al., 2017; Thongtham & Kristensen, 2005). Higher food quality also increases the molting frequency and reproductive effort of mangrove crabs, supporting secondary productivity (Micheli, 1993; Riley et al., 2014). By increasing nitrogen content in basal food sources and primary consumers, we show that seabird nutrient subsidies contribute to larger sizes of herbivorous and omnivorous mangrove crabs. Links between larger sizes of consumers and seabird nutrient enrichment of food sources have also been documented in lizards (Richardson et al., 2019) and herbivorous reef fish (Benkwitt et al., 2021). Crabs are important components of mangrove fisheries worldwide (Rönnbäck, 1999), and they are often regulated by catch-size limits (Glaser & Diele, 2004). Research in coastal wetlands shows that nutrient subsidies increase fisheries' landings of mobile invertebrates. Nutrient inputs enrich food sources and increase the growth and reproduction of exploited mangrove species, thereby enhancing fisheries yields (Breitburg et al., 2009). Although additional data on crab abundance would allow stock assessment, our results provide a preliminary indication that seabird nutrient subsidies can promote mangrove crab fishery productivity.

Additionally, crab fisheries' productivity and landings correlate positively with mangrove coverage (Aburto-Oropeza et al., 2008; Carrasquilla-Henao et al., 2013; Manson et al., 2005). On Aldabra, seabird nutrient subsidies boost mangrove forest nutrient status (Appoo, Bunbury, et al., 2024), and increases in mangrove extent coincide with seabird colonies (Constance et al., 2021). By improving mangrove forest health, seabird nutrient subsidies can indirectly enhance not only mangrove crab fisheries but also other income-generating activities like ecotourism and critical services such as coastal protection, suggesting that seabird populations can play an important role in promoting mangrove ecosystem service delivery (Plazas-Jiménez & Cianciaruso, 2020). In contrast, we found no relationship between seabird nutrient subsidies and size of littorinid gastropods. This may be due to differences in species composition of littorinids sampled across sites. Moreover, littorinid gastropod growth depends on the secretion of calcium carbonate and is associated with shell morphology (form and thickness; Riascos & Guzman, 2010): Fast-growing littorinid snails have thin, spherical shells to accommodate larger body mass, while slower growing individuals have thick, cone-shaped shells (Kemp & Bertness, 1984). Improving the taxonomic resolution of littorinid gastropods, as well as collecting additional data on shell allometry or tissue dry weight, would help determine any seabird nutrient subsidy effect on gastropod sizes.

Seabird nutrient subsidies had similar impacts on the isotopic niches and resource contributions of the two macroinvertebrate herbivores. At seabird sites, littorinid gastropods and sesarmid crabs exhibited broader isotopic niches, shifting toward more enriched δ¹⁵N, and had greater overlap, attributed to their similar resource use. Epiphytic macroalgae and guano constituted >50% of their relative resource contributions, in stark contrast to their relative resource contributions at non-seabird sites, where littorinid gastropods consumed 77% mangrove leaves, and sesarmid crabs 41% mangrove leaves and 36% SOM. The preference for epiphytic macroalgae as a resource for the two herbivores at seabird sites is likely related to the higher nutritional content of epiphytic macroalgae as a result of enrichment by seabird nutrient subsidies (Kolb et al., 2010). Littorinid gastropods and sesarmid crabs play important roles in recycling mangrove nutrients and organic matter (Ferreira et al., 2024). The shift in resource use suggests that seabird nutrient enrichment can potentially reduce mangrove consumption and nutrient cycling by littorinid gastropods and sesarmid crabs. Additional data on invertebrate abundance, community composition, and mangrove herbivory rates are needed to explore this link. Mangrove herbivory might be increased for other feeding guilds; leaf-eating insects in seabird-subsidized mangroves in Florida had higher feeding rates, which led to greater losses of mangrove biomass (Onuf et al., 1977), indicating increased recycling of mangrove carbon by this group of herbivores. Furthermore, our study sites are nitrogen-limited (Appoo, Bunbury, et al., 2024) and fertilization experiments have demonstrated that nitrogen enrichment increases mangrove herbivory in such environments (Feller et al., 2007). Improving the taxonomic resolution of littorinid gastropods and epiphytic macroalgae samples would reduce potential sources of error related to taxonomic differences between sites and strengthen our results. In addition, expanding our study to include more herbivore feeding guilds would provide a more holistic overview of the impacts of seabird nutrient subsidies on mangrove nutrient cycling.

Food resources for portunid crabs at seabird sites comprised comparable relative proportions of BMI (37%), sesarmid crabs (20%), guano (17%), and littorinid gastropods (16%). In contrast, at non-seabird sites, portunid crabs consumed mainly BMI (51%). The niche overlap of portunid crabs with mangrove-dwelling macroinvertebrates was also slightly higher at seabird sites than at non-seabird sites. Together, this suggests that at seabird sites, portunid crabs foraged closer to the mangroves, where resources were of higher quality due to seabird-derived nutrients. Conversely, in the absence of seabirds, portunid crabs likely foraged further away from the mangroves, indicated by their larger isotopic niche, which
shifted toward more enriched δ¹³C values (reflecting a marine carbon signature, as opposed to depleted δ¹³C values associated with terrestrial carbon). Additionally, mixing model results suggests that at non-seabird sites, portunid crab diet primarily consisted of prey feeding on BMI, such as shrimps, hermit crabs, and fiddler crabs commonly found in the intertidal zone (Cannicci et al., 1996; Le et al., 2017). This suggests that at non-seabird sites, portunid crabs likely have a reduced role in the mangrove food web dynamics and contribute more to the intertidal food web. Our analysis included global averages of BMI isotopic ratios from semiarid mangroves, and direct measurements are needed to strengthen our findings.

Consistent with our results, studies in Mediterranean coastal ponds subsidized by seabird guano show that invertebrate communities shift their resource use toward enriched sources, and the authors suggest that seabird nutrient enrichment leads to high trophic redundancy and simplification of food webs (Vizzini et al., 2016). High trophic redundancy may also indicate high functional redundancy, that is, more species with similar functional roles (Agusto, 2021). Theoretical predictions reveal that food webs with high trophic and functional redundancy are more resilient, meaning that if one species were to go extinct, their trophic or functional role would be maintained by other species within the same feeding guild (Borrvall et al., 2000; Sanders et al., 2018). In our study, two macroinvertebrate herbivores with different feeding guilds (surface grazer and folivore) switched to similar trophic habits at seabird sites, suggesting the potential for similar shifts of other species within the same feeding guilds. This implies that seabird nutrient subsidies may contribute to functional redundancy of macroinvertebrate fauna and, consequently, the trophic resilience of mangrove food webs. This is particularly important in the Western Indian Ocean, where mangrove invertebrate communities exhibit low functional redundancy and high functional vulnerability (Cannicci et al., 2021). Additional assessments including more trophic guilds, along with mangrove invertebrate abundance and diversity, are needed to explore and validate this link.

## CONCLUSION

Invertebrate assemblages underpin mangrove health, functioning, and ecosystem services. Our study provides insights into the impacts of seabirds within mangroves by shedding light on the trophic response of functionally important macroinvertebrate fauna to seabird guano contributions. Seabird nutrient subsidies enhance the nutritive value of basal food sources and increase sizes of mangrove

crabs, suggesting that seabird populations can promote mangrove crab fishery productivity and benefit the provisioning of mangrove ecosystem services. Enrichment of basal resources caused a shift in resource use among primary and secondary mangrove macroinvertebrate consumers, altering trophic interactions with potential consequences on mangrove ecosystem processes. Further studies addressing higher trophic levels, such as mangrove fish communities, are needed to elucidate the extent of the effects of seabird nutrient subsidies on tropical coastal food webs and fisheries.

## AUTHOR CONTRIBUTIONS

**Conceptualization:** Jennifer Appoo, Nicholas A. J. Graham, Sébastien Jaquemet, and Nancy Bunbury. **Methodology:** Jennifer Appoo and Nancy Bunbury. **Data collection:** Jennifer Appoo and Christopher W. Jones. **Formal analysis:** Jennifer Appoo. **Writing (original draft):** Jennifer Appoo. **Writing (review):** Jennifer Appoo, Nicholas A. J. Graham, Christopher W. Jones, Sébastien Jaquemet, and Nancy Bunbury.

## ACKNOWLEDGMENTS

We thank the Seychelles Islands Foundation for providing administrative and logistical support during the fieldwork, especially Frauke Fleischer-Dogley, Ervin Ally, Elma Balette, Sebastien Cowin, Nikita Pothin, Michelle Jones, Annabelle Cupidon, Guilly Mellie, Anna Koester, and Francis Solomon. Jennifer Appoo was supported by a doctoral fellowship from the Région Réunion. Funding was provided by the African World Heritage Fund to Jennifer Appoo, PADI Foundation to Jennifer Appoo, and Bertarelli Foundation as part of the Marine Science Programme to Nicholas A. J. Graham. Fieldwork and ethical approval were provided by the Seychelles Bureau of Standards (permit number A0157).

## CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

## DATA AVAILABILITY STATEMENT

Data (Appoo, Graham, et al., 2024) are available from Dryad: https://doi.org/10.5061/dryad.dncjsxm6m.

## ORCID

Jennifer Appoo https://orcid.org/0000-0002-3980-9435

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## SUPPORTING INFORMATION

Additional supporting information can be found online in the Supporting Information section at the end of this article.

**How to cite this article:** Appoo, Jennifer, Nicholas A. J. Graham, Christopher W. Jones, Sébastien Jaquemet, and Nancy Bunbury. 2024. "Seabird Nutrient Subsidy Alters Size and Resource Use of Functionally Important Mangrove Macroinvertebrates." *Ecosphere* 15(12): e70121. https://doi.org/10.1002/ecs2.70121