Abstract
Many species of seabird ingest or are provisioned with pumice stones, buoyant volcanic rocks that are thought to aide in digestion, occasionally during times of poor prey availability. Unlike other indigestible matter, like plastics, the effect of pumice on chick growth, its relationship with ingested plastics, and variation among years has not yet been examined. We analysed the amount of ingested pumice from 739 Flesh-footed (Ardenna carneipes) and 173 Wedge-tailed Shearwaters (A. pacifica) from Lord Howe Island, Australia sampled using stomach lavage between 2011 and 2022. The total mass of ingested pumice was positively related to the mass of ingested plastics in Flesh-footed, but not Wedge-tailed Shearwaters, but not when using mean stone mass. Pumice mass did not vary over time, except for one higher year for each species (2016 for Flesh-footed Shearwaters and 2014 for Wedge-tailed Shearwaters), and there was no effect of pumice mass on chick body size at fledgling. Our results are consistent with the coexistence over geological time of seabirds and floating pumice, and future work should focus on aspects of retention in the digestive system and potential interactions with and efficacy in the presence of novel materials, like plastics.
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Introduction
Large rafts of pumice stones are frequently recorded in marine and coastal environments following volcanic eruptions (e.g., Coombs and Landis 1966; Bryan et al. 2004; Jutzeler et al. 2014) with individual eruptions producing > 3 trillion stones in a single day (Jutzeler 2014). Pumice rafts from a single volcanic event can extend over many hundreds of square kilometers (Jutzeler et al. 2014; Ohno et al. 2022) and commonly include stones that range in size from around 1 cm to > 1 m in diameter (Risso et al. 2002). Because pumice is less dense than seawater, the stones float and can be transported vast distances by ocean currents (Bryan et al. 2012). During this time, pumice can accumulate a biofilm (layer of bacteria, algae, and other microorganisms adhered to the surface) and sink or otherwise disappear from the ocean’s surface (i.e., deposited on beaches), typically within a few months to years (Vella and Huppert 2007). Despite being distributed across ocean basins, pumice stones have chemical signatures that are unique to their origin (i.e., volcanic eruption) allowing the provenance of stones recovered off distant beaches to be determined (Ward and Little 2000).
Scientists have long recorded pumice stones in the stomachs of wild animals and people (Baker 1956), with physician Robert Mayne coining the term “gastrolith” in 1860 (Mayne 1860), and in birds these are often called “gizzard stones” (McCann 1939). These stones of various sizes and composition have been ingested by marine and terrestrial bird species (Robards 1993; Wings 2007) and their ancestors, including dinosaurs (e.g., O’Connor et al. 2018) and the extinct Moa (Rowley 1878). Among seabirds, the ingestion of pumice or the presence of gastroliths is widespread, covering penguins, albatrosses, petrels, storm-petrels, skuas, and auks (Simpson 1965; Robards 1993; Beaune et al. 2009). It’s often assumed that pumice is consumed to assist with digestion (Ziswiller and Farner 1972), with small stones frequently found in the gizzard (the muscular compartment of the stomach; Blight and Burger 1997), but little is known about the factors that influence the consumption and subsequent retention of pumice in seabird species, or how adults may provision them to their nest-bound chicks. Pumice is often recorded in seabird stomachs alongside other, non-digestible items such as plastics (Kenyon and Kridler 1969) in part because the at-sea distributions of plastic and pumice overlap, particularly along the boundary of ocean currents and other high productivity zones (Bryan et al. 2004) where seabirds are known to forage (Balance et al. 2001).
Exposure to ingested plastics causes scar tissue formation in the proventriculus and other organs (Charlton-Howard et al. 2023), and the loss of structures in the stomach that are essential to digestive processes (e.g., rugae and tubular glands; Rivers-Auty et al. 2023). However, these detrimental changes were not recorded in birds with only ingested pumice, suggesting this pathology is unique to plastics and providing evidence for an evolutionarily beneficial (or at least neutral) relationship between the birds and the consumption of pumice (Rivers-Auty et al. 2023). This agrees with historical studies where significant quantities of pumice, but not plastic, have been recorded in seabirds with no negative effects (e.g., Simpson 1965).
Despite a long history of documenting the presence of gastroliths more broadly, and pumice in particular, there has not yet been an attempt to quantify what effect, if any, ingesting pumice may have on seabird growth, its relationship with other indigestible matter, such as plastics, and how its prevalence and abundance in seabirds may be changing over time. We hypothesized that (1) birds with more ingested plastic would also have more ingested pumice as adults who fed their chicks plastic would be less discriminatory among “non-food” items, (2) the mean mass of pumice per chick would be constant over time, reflecting a long relationship between birds and pumice through geological time, and (3) pumice would not affect chicks’ growth and therefore be unrelated to morphometrics of fledglings, given their evolution has been presumably been consistently influenced by the presence of pumice in the oceans.
Methods
Between 2011 and 2022, we collected ingested pumice as part of a long-term study of plastic ingestion by Flesh-footed (Ardenna carneipes) and Wedge-tailed (A. pacifica) Shearwaters on Lord Howe Island, New South Wales, Australia (31.53ºS, 159.07ºE; Lavers et al. 2018, 2021). Both species breed September through May, with chicks departing the nest (fledging) in late-April or early-May.
Briefly, birds were lavaged (stomach flushing) using ambient temperature seawater (approx. 100 and 150 ml for Wedge-tailed and Flesh-footed Shearwaters, respectively) until they emitted their stomach contents (proventriculus only), and then released back at the point of capture. We sampled fledging chicks (80–90 days old) exclusively. Pumice from each bird was washed, dried, enumerated, and weighed using an electronic balance to the nearest 0.0001 g. Other types of stones, such as calcarenite or basalt (both found on Lord Howe Island), are rarely detected in the birds and were readily distinguishable by colour, texture, and flotation. For a description of the methods on recording ingested plastics and details of the plastic items recovered from these same birds, see Lavers et al. (2021). As all plastic and pumice were visually examined while in the field, the minimum particle size is 1 mm. We also calculated the mean mass of pumice stones per individual (calculated as the total mass/number of stones).
At the time of capture, we also recorded the birds’ mass (± 10 g) using a spring balance, flattened and straightened wing chord (± 1 mm) using a stopped ruler, and head + bill and culmen length (± 0.1 mm) using Vernier calipers.
All statistical analyses were conducted in R 4.2.1 (R Core Team 2022). We examined the relationships between the mass of ingested pumice and the mass of ingested plastics, birds’ morphometrics (as a proxy for growth rate), and the mass of pumice ingested over time (Flesh-footed Shearwaters: 2011–2022; Wedge-tailed Shearwaters: 2014–2021) using a series of general linear models with Tukey’s post-hoc tests for multiple comparisons when linear models were significant. Pumice mass was log-transformed to improve normality of the residuals, which were examined visually along with Q-Q plots. We opted to use untransformed morphometrics given the narrow age range of individuals in our study, and the challenges of using unverified indices of body condition (Schamber et al. 2009) which perform equally well as variable reduction methods (Labocha and Hayes 2012). Results were considered significant when p < 0.05.
Results
In total, we had data on pumice ingestion for 739 Flesh-footed and 173 Wedge-tailed Shearwaters (Table 1, Fig. 1). For Flesh-footed Shearwaters, after accounting for sampling year, the mass of ingested pumice was positively related to the mass of ingested plastics (F1,613 = 289.45, p < 0.001; β ± SE = 0.2029 ± 0.0128; Fig. 2), with significant variation among years in the mass of pumice ingested, though this was strongly driven by 2016 and in most years the relationship was flat (Fig. 2). There was no relationship between the mean mass of pumice and ingested plastic mass (F1,121 = 2.50, p = 0.12).
In Wedge-tailed Shearwaters, there was no relationship between the ingested mass of plastics and pumice (F1,150 = 0.02, p = 0.89; Fig. 3), and like in Flesh-footed Shearwaters, no relationship between the mean pumice mass and the mass of ingested plastics (F1,65 = 0.28, p = 0.60). Examining temporal trends revealed significantly greater mass of pumice in only one year for Flesh-footed Shearwaters (2016; F10,617 = 6.46, p < 0.001; Fig. 4) with all other years similar, whereas for Wedge-tailed Shearwaters this was driven by higher amounts of pumice in 2014 (Fig. 5).
There was no relationship between pumice mass and Flesh-footed Shearwater chick mass (F1,592 = 0.23, p = 0.63), head + bill (F1,581 = 0.12, p = 0.73), culmen (F1,580 = 0.03, p = 0.86), or wing chord (F1,574 = 1.81, p = 0.18). For Wedge-tailed Shearwaters, there was also no relationship between ingested pumice mass and chick mass (F1,155 = 0.62, p = 0.43), head + bill (F1,119 = 0.001, p = 0.97), culmen (F1,119 = 0.31, p = 0.58) or wing chord (F1,119 = 0.04, p = 0.84).
Discussion
We found that for both Flesh-footed and Wedge-tailed Shearwaters, the mass of pumice provisioned to chicks did not change significantly among years, with a few exceptions (Figs. 2, 3), and that the quantity of ingested pumice mirrored the amount of plastic consumed by individual birds, meaning birds with more plastic contained, on average, more pumice (Fig. 2). The ingestion of larger quantities of plastic did not, however, equate to birds consuming larger pumice stones (measured by the mean stone mass per bird), meaning some birds were eating more pumice, but not necessarily larger pieces.
Unlike in Flesh-footed Shearwaters, there was no relationship between the mass of ingested plastics and pumice in Wedge-tailed Shearwaters. Wedge-tailed Shearwaters generally have a lower frequency of occurrence of plastics (19–40%; Lavers et al. 2018) than Flesh-footed Shearwaters (37–85%; Lavers et al. 2021), and the mean mass of plastic ingested (0.01–0.06 g) is also much lower than in Flesh-footed Shearwaters (0.04–2.93 g). Given this lower variability, the smaller amount of ingested pumice and plastics relative to our ability to detect them, and their smaller size (ca. 400 g; Marchant and Higgins 1990) the lack of a relationship is perhaps not surprising. Furness (1985) also found no relationship between pumice and other indigestible matter in seabirds from Gough Island while (Ryan 1988) found that for Blue Petrels (Halobaena caerulea) on the Prince Edward Islands, the relationship between ingested plastics and pumice was present only in the post-breeding period, and not for pre-breeding adults, presuming this was related to the flux of plastics through seabirds as parents provision chicks. This flux is still poorly understood (Ryan 2015), and further study into factors influencing gut retention times of ingested non-food items would help us understand the potential impacts of decreasing prey availability and increasing plastic pollution in the birds’ environment.
Overall, quantity of pumice ingested by the birds was consistent over time, except for elevated quantities in 2014 (Wedge-tailed Shearwaters) and 2016 (Flesh-footed Shearwaters). As both species have broadly similar foraging behaviours and feed at the same time of year (Reid et al. 2012; Miller et al. 2018), it’s unlikely that these influxes represent a novel source of pumice (e.g., an underwater eruption). More likely, they could be the rest of particularly poor foraging conditions or prey availability. In neither year was chick body condition notably poorer than others (Lavers and Bond 2023; authors’ unpublished data), though when birds experience prey shortages, they may be more likely to ingest material like pumice (Roman et al. 2021), though this may not be universal (Furness 1985). The 2012 Havre eruption (Jutzeler et al. 2014) that was thought to be the source of ingested pumice by shearwaters beach-washed in Queensland in 2013 (Roman et al. 2021) was not detected in our dataset, despite being only a few hundred kilometres south on Lord Howe Island. Investigations into the diet, chick provisioning behaviour, differences in parental effort between sexes, and feeding strategies of the shearwater populations in the Tasman Sea would potentially help our understanding of the differences between them.
One key difference between our study and Roman et al. (2021) is that in our case, birds were nest-bound chicks who had been provisioned by their parents. In many seabirds with biparental care, there is often a trade-off between self-maintenance and caring for offspring (Clark and Ydenberg 1990), and in poorer conditions adults will favour their own survival. With generally high annual adult survival and low fecundity (1 egg/year), this is the most evolutionarily favourable strategy for shearwaters (Hamer et al. 2002). In years with higher pumice mass in chicks, it suggests that adults may have been at the threshold of being able to provision young, which occasionally necessitated returning with indigestible matter. This is borne out by the fact that Flesh-footed Shearwaters had the highest mean mass of ingested plastics in 2016 (2.93 g; Lavers et al. 2021), though this was not the case for Wedge-tailed Shearwaters, where the amount of ingested plastics in 2014 was about average (0.01 g; Lavers et al. 2018).
The ingestion of pumice did not negatively impact the body condition of either shearwater species. This outcome likely reflects the relationship of seabirds ingesting pumice throughout geological time with pumice and other small stones long thought to aid in the digestion process (McCann 1939). In contrast to other similarly sized, non-digestible materials consumed by seabirds such as plastics, the presence of pumice in seabirds’ proventriculus is not associated with harm to the surrounding tissues (Rivers-Auty et al. 2023) although large quantities may interfere with the passage of food (Kenyon and Kridler 1969) or otherwise contribute to dietary dilution (reduced feeding frequency or volume due to the presence of non-food items in the stomach; Roman et al. 2020). The highly porous nature of pumice means the stones could act as transporters of chemicals, biofilm, or particulate matter which could impact shearwater physiology, however given the evolutionary time over which birds and pumice have coexisted, and the small volumes or concentrations relative to other sources (e.g., prey or plastics) suggest this effect would be minimal if even observable.
We could find no data describing the co-occurrence of pumice and plastics at sea. Both pumice and plastics are transported by oceanic winds, waves and currents and accumulate a biofilm that can affect vertical transport within the water column (Rummel et al. 2017). While pumice is likely to persist in the marine environment for a shorter duration than plastic, both likely overlap in space and time, especially within oceanic gyres and along convergence zones where floating ocean detritus has been demonstrated to accumulate (Thiel and Haye 2006; van Sebille et al. 2020). Many of these same ocean regions are also biodiversity hotspots (Arcos et al. 2012; Fossi et al. 2017), increasing the chance of foraging seabirds and other wildlife interacting and potentially ingesting both plastics and pumice.
Together our results show that pumice provisioned to and retained by chicks until fledging has no negative consequences, but that in some species it may be related to the amount of other indigestible material present, such as plastics. The benefits of pumice at the individual level in seabirds, its residency time, and how it might interact with more novel non-food items, like plastics, is an area for future study.
Data availability
Data are available on figshare: https://doi.org/10.6084/m9.figshare.21664256.
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Acknowledgements
The authors acknowledge the traditional custodians of the land and waters where this paper was written, the muwinina people of nipaluna (Hobart, Australia) and Wudjari people of Kepa Kurl (Esperance, Australia), and celebrate the role that Indigenous people have played as the first scientists and conservationists of this land. Samples were collected with the permission of the Lord Howe Island Board (permit no. LHIB 07/12, 02/14, and 07/18) and New South Wales Office of Environment & Heritage licence (no. SL100619 and SL102382). Logistical support was provided by the Australian Bird and Bat Banding Service and Lord Howe Island community, especially C. Woods, J. Gilligan, T. Adams, L. Brice, and J. & C. Shick. Assistance in the field was provided by generous volunteers, particularly P. Clive, the Two Hands Project (S. Stuckenbrock & P. Sharp) and members of the Adrift Lab team. G. Henderson kindly provided the photos in Figure 1. Comments from three anonymous reviewers improved earlier drafts.
Funding
Special thanks to Detached Cultural Organization (P. Clive), Sea World Research & Rescue Foundation (SWR/4/2015), Sydney Sea Life Foundation, Natural History Museum, Trading Consultants Ltd (V. Wellington), L. Brice, L. Mortensen (Ocean Plastic Relay – Day of 30), C. Noone, and the W.V. Scott Charitable Trust for providing funding for our long-term monitoring.
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JLL—Conceptualization, Data curation, Funding acquisition, Investigation, Project administration, Writing-Original draft. AL. Bond—Conceptualization, Data curation, Funding acquisition, Investigation, Project administration, Formal analysis, Writing-Original draft.
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Lavers, J.L., Bond, A.L. Pumice ingestion in seabirds: interannual variation, and relationships with chick growth and plastic ingestion. Mar Biol 170, 55 (2023). https://doi.org/10.1007/s00227-023-04203-6
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DOI: https://doi.org/10.1007/s00227-023-04203-6