Results and Discussion

Reports of MMEs have been increasing through time for all taxa (Fig. 1). However, contemporaneous heightened scientific awareness of MMEs coupled with an overall increase in total scientific productivity (Fig. 1 and SI Appendix, Fig. S1) could generate a perceived increase. This putative publication bias is a well-known phenomenon when dealing with rare events occurring in time series data, akin to the challenge of distinguishing ongoing epidemics from “epidemics of discovery” (19). Notably, however, more than half of the variation (mean = 54.5%; range = 15–84%) in changes in the occurrence of MMEs through time was not explained by increases in publication output alone (SI Appendix, Fig. S2). MMEs were only sporadically reported during the late nineteenth century and early part of the 1900s; since the 1940s, however, MMEs have been documented consistently for birds, fishes, mammals, and marine invertebrates on all continents and in all major biomes. Overall, fishes were the largest contributor of reported MMEs, accounting for 56% of all documented MMEs (Fig. 1). Our analysis also captures a sharp increase in the occurrence of amphibian and reptile MMEs beginning in the 1970s, coincident with the growing awareness of global amphibian declines (20), and more recently, declines in reptiles (21). The recent declines in the occurrence of MMEs since 2000 for all groups but reptiles (Fig. 1) are likely a result of reporting delays between when events occur and when they are reported in the literature (SI Appendix, Fig. S3), and statistically accounting for these delays reduces the extent of recent declines in MME occurrence (SI Appendix, Fig. S4). Such delays may increase in length as ecologists continue to use older datasets.

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Fig. 1.

Occurrences of animal MMEs and taxon-specific publication trends through time. Colored bars indicate the number of events during a 5-y interval (e.g., 1940 stands for the 1940–1944 period), and dashed lines show trends in the total number of papers published each year for each taxon. For all taxa, the increase in the number of MMEs is coincident with an increase in the number of publications (SI Appendix, Fig. S1).

Our analysis reveals that the magnitudes of MMEs are changing through time, as measured by the number of animals that died during each event (Fig. 2). Interestingly, changes in the magnitude of MMEs are variable among animal taxa: magnitude increases for birds, marine invertebrates, and fishes; remains invariant for mammals; and decreases for amphibians and reptiles, despite substantial variation around these patterns (Fig. 2). With the exception of reptiles and amphibians, in which a slight quadratic trend in the magnitude of MMEs is present, a nonparametric local regression of these data reveals comparable trends (SI Appendix, Fig. S5). These trends in the number of individuals killed per MME likely do not result from a publication bias, as the observed trends for all taxa proved robust when the dataset was reanalyzed by resampling to account for increased MME reporting through time (SI Appendix, Fig. S6) (22). We note that the temporal patterns of reptile and marine invertebrate MMEs should be interpreted with caution because of their comparatively low sample size. Overall, taxon, cause, and year explained the largest amounts of variance in the magnitude of MMEs (21.0%, 7.4%, and 4.9%, respectively; multiple linear regression: F_21,770 = 18.3; P < 0.001).

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Fig. 2.

Magnitude of animal MMEs through time. Each point is a single MME (n = 727 total events). Dashed lines represent statistically significant slopes, shading demarcates slope 95% confidence intervals, and hatched shading indicates extrapolation of regressions before the first reported MME.

The positive trends in MME magnitude for fishes, birds, and marine invertebrates also runs counter to the tendency for scientists to report the largest, most obvious events, whereas less-obvious events are typically increasingly reported when scientific awareness and allocated effort escalate (23). As such, the average increases in MME magnitude for birds, fishes, and marine invertebrates, which on average tended to increase by 0.22, 0.33, and 0.60 orders of magnitude per decade, respectively, are surprising, given the increased MME reporting through time (Fig. 1).

Although the proportion of the animal population removed during an MME remains the most widespread approach for defining an MME (2, 3, 14), only 9.6% of published MMEs reported information on how MMEs affect population sizes (SI Appendix, Fig. S7). This lack of data limits our ability to resolve temporal patterns in the population-level consequences of MMEs. However, the available data suggest that reported MMEs frequently remove a substantial proportion of animal populations, including up to 100% of the population (SI Appendix, Fig. S7). Because we have no reason to suspect that population sizes for these taxa have consistently been increasing through time, the positive trends in MME magnitude documented in numbers of individuals for fishes, birds, and marine invertebrates likely indicate an increase in the proportion of the population being removed.

The differences in MME magnitude among animal taxa may also highlight an important relationship between MMEs and population demographics. Among vertebrate taxa, amphibians, reptiles, and mammals contain the largest proportion of species that are threatened, according to the International Union for Conservation of Nature (IUCN) Red List, and birds and fishes contain proportionally fewer threatened species (24). Thus, one possibility is that the tendency for MME magnitude among certain taxa to increase and then decrease over time may reflect an overall recent decrease in the size of their extant populations (Fig. 2 and SI Appendix, Fig. S5). Intriguingly, the recent patterns of amphibian and reptile MME magnitude (SI Appendix, Fig. S5) support this hypothesis; however, the comparatively small sample sizes for these taxa and lack of population-specific data suggest caution is warranted in this interpretation. One extreme example of this mechanism is the 1983 sea urchin Diadema antillarum MME, which was likely caused by a waterborne pathogen that removed an estimated 99% of all Diadema from the Caribbean. Such a large-scale event precludes the occurrence of similarly large die-offs in the near future (25) and may be a precursor to local and regional defaunation (26, 27).

Across all animal taxa, causes of MMEs were most often associated with disease (Fig. 3; 26.3%) and were attributed to viral (44.5%), bacterial (18.3%), and fungal infections (12.2%). Human perturbation was the second most common cause of MMEs, accounting for 19.3% of total MMEs, mainly from point source environmental contamination (42.5%). Biotoxicity was the third leading cause of MMEs (15.6%), primarily resulting from toxin-producing cyanobacteria and dinoflagellates that dominate marine and freshwater harmful algal blooms. Processes directly influenced by climate (weather, thermal stress, oxygen stress, starvation) also contributed to the occurrence of MMEs and accounted, collectively, for 24.7% of known cases.

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Fig. 3.

Causes of MMEs and associated variation in the magnitude of events for different causes. (Left) Bars quantify the total number of mortality events for a given cause, and lines within the bars indicate the relative change in the occurrence of each cause from 1940 to 2009. *Significant temporal trends. (Right) Variation in the magnitude of mass mortality across causal categories after taking into account taxon-specific temporal trends. Shown are the residuals (mean ± 1 SE) from an ANCOVA model, including taxa and year; that is, a model that describes the expected mortality magnitude without taking into account the causes. Causes with larger magnitudes of death than the average will have positive residuals (e.g., starvation), whereas causes with smaller magnitude than the average will have negative residuals (e.g., O₂ stress).

The causes of MMEs also exhibit shifts through time, but importantly, the causes of MMEs do not change uniformly through time for all taxa. Overall, infectious disease, biotoxicity, and multiple stressors were the most rapidly intensifying causes of MMEs, increasing from 0–33%, 5–18%, and 0–8% of reported MMEs from the 1940s to the 2000s, respectively (Fig. 3). One explanation for these observed shifts is that technological improvements have enabled increased detection of disease and biotoxicity, which rely heavily on laboratory-based methods for detection (28). As such, increased efforts in disease and biotoxicity research could also produce such a pattern. However, if heightened awareness were responsible for these patterns, we would expect to see a positive relationship between the number of publications including disease and biotoxicity as keywords and the proportion of MMEs attributed to these causes. Analysis of this relationship shows that although scientific attention to these topical areas has increased, these increases are rarely coincident with the proportion of MMEs attributable to a particular cause for a particular period (SI Appendix, Fig. S8). Thus, although we suspect that heightened awareness of these issues has increased, both disease and biotoxicity likely remain important causes of MMEs that have changed through time.

However, not all taxa exhibited uniform increases in MMEs attributed to disease and biotoxicity (Fig. 4; ANOVA year × cause × taxa; F_45,210 = 1.47; P = 0.038). Whereas fishes have had consistent proportions of MMEs attributed to disease and biotoxicity, birds have only recently seen an increase in the frequency of MMEs attributed to these causes. Moreover, fishes and birds exhibited sustained instances of MMEs caused by direct human perturbations, but mammal MMEs only included such causes in the last three decades (Fig. 4). Therefore, the observed shifts in MME causes might not be driven entirely by reporting or by a detectability bias, yet the varied emphasis put forth by the scientific community on these topics complicates this interpretation (SI Appendix, Fig. S8). Nevertheless, it remains possible that both infectious disease and biotoxicity caused by toxic algal blooms, which are commonly associated with recent land-use alterations and climate variability (29, 30), may increasingly cause MMEs, rather than simply being chronic and ongoing perturbations to natural systems.

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Fig. 4.

Relative frequency of each cause of mortality for each taxon through time. Bars indicate the relative frequency of an MME cause for particular taxa for each decade. Decades are defined by their start year (e.g., 1940 represents the period 1940–1949).

In addition, recent shifts in MME causes may result from underlying patterns in the occurrence of MMEs within certain taxa. For example, amphibians and reptile MMEs are overwhelmingly associated with bacterial, fungal, and viral infections (Fig. 4), and reports of amphibian and reptilian MMEs sharply increased during the past several decades (Fig. 1), thus increasing the proportion of all MMEs attributed to disease.

Similarly, the overall relative occurrence of thermal stress as a casual factor of MMEs has been declining through time for birds, fishes, and marine invertebrates (Fig. 4). A closer examination of the patterns associated with thermal stress reveals that this trend resulted from reductions in the occurrence of cold thermal stress events (SI Appendix, Fig. S9), whereas events related to hot thermal stress, although infrequent (n = 6 events), have only appeared since the 1980s. The decrease in MMEs attributed to cold thermal stress may relate to the concurrent reductions in the severity of winter temperatures (18), and it is likely that trends toward increases in summer temperatures may result in an increased occurrence of hot thermal stress events in the future (31). Such trends in thermal stress events raise an important consideration regarding the underlying mechanisms of MMEs driven by environmental forces. MMEs arising from changes in the abiotic environment either may arise from large changes in environmental conditions (e.g., temperature or toxin concentration) or, alternatively, may arise from smaller environmental changes that have a disproportionately large negative fitness effect if biological thresholds are reached (32, 33). Thus, both incremental and episodic environmental change may contribute to the recent increased occurrence of MMEs (Fig. 1).

Interestingly, the causes of MMEs also varied in their associated magnitudes. After taking into account variation among taxa in the temporal trends in MME magnitudes (Fig. 2), we found that multiple stressors, starvation, and disease were associated with the largest MME magnitudes, whereas oxygen stress, toxicity, and desiccation were associated with the smallest MME magnitudes (Fig. 3). Identifying the factors generating variation in MME magnitude is important because it may improve predictions of MME magnitudes, assuming the current trends in MME causes persist. However, it is possible for MME causes to shift independent of trends in MME magnitudes. Mammals exhibited no directional changes in MME magnitude through time (Fig. 2), yet the occurrence of mammal MMEs caused by desiccation decreased through time (Fig. 4) and resulted in the overall decrease in desiccation-related MMEs across taxa (Fig. 3).

Overall, the interpretation of patterns related to MME causes or taxa should be considered in the context of sources of bias that may be present. The high proportion of MMEs reported in North America and Europe (SI Appendix, Fig. S10) reflects a reporting bias toward areas containing high human densities and areas where ecologists often conduct fieldwork (4, 34). Moreover, certain causes of MMEs are likely underrepresented in the publication records as a result of being difficult to detect (29). For example, causes of mortality affecting aquatic taxa are likely underreported because dead organisms can sink out of sight (7) or occur in the open ocean. In addition, losses of highly gregarious organisms or organisms that dominate biological communities in terms of relative abundance may be reported more often relative to losses of rare organisms, for which losses may even go undetected. Finally, the geographic location of MMEs likely determines whether it is encountered, and thus reported; for example, higher temperatures in tropical ecosystems can accelerate decomposition rates, shortening the window within which MMEs can be observed.

In conclusion, our analysis of published animal MMEs indicates that the magnitude of MMEs has been undergoing taxon-specific shifts and that MMEs associated with multiple stressors and disease, which are associated with the largest MME magnitudes, are increasing in frequency. However, it is difficult at this time to determine how much of this increase reflects improved detection capabilities and a greater emphasis on these research topics. Determining whether or not the upswing in the occurrence of MMEs is a real phenomenon or simply a result of increased awareness remains a critical challenge that needs to be addressed. Such results, combined with lack of studies measuring MMEs using population-level data, highlights the need for an improved program for monitoring MMEs. Beyond data standardization, we encourage increased coordination of data collection networks such as citizen scientist contributions, state and federal agencies, and academic scientists. At this time, the vast majority of MMEs are presented in newspapers (7) and do not find their way into the primary literature. Ultimately, enhancing the study of MMEs will enable an appropriate integration of rare demographic processes into established ecological and evolutionary theory. Although MMEs are a natural occurrence, as we continue to proceed through an era of dramatic changes to Earth’s physical (17, 18) and biological systems (5, 29), a heightened awareness and robust detection network (6, 29) may be warranted.