SciELO - Scientific Electronic Library Online

 
vol.49Familias de micromoluscos durante 2 periodos contrastantes en Bahía de los Ángeles, golfo de California, MéxicoComposición y diversidad espaciotemporal de la comunidad de aves acuáticas en la laguna de las Ilusiones, Tabasco, México índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados

Journal

Artigo

Indicadores

Links relacionados

  • Não possue artigos similaresSimilares em SciELO

Compartilhar


Ciencias marinas

versão impressa ISSN 0185-3880

Cienc. mar vol.49  Ensenada Jan./Dez. 2023  Epub 08-Dez-2023

https://doi.org/10.7773/cm.y2023.3361 

Articles

Decline of one of the southernmost northern elephant seal (Mirounga angustirostris) colonies and its relationship with a warm sea environment

Eunice Donají Rodríguez-Rafael1 
http://orcid.org/0000-0003-2547-9727

María de la Concepción García-Aguilar2 
http://orcid.org/0000-0002-7451-9361

Felipe Galván-Magaña1 
http://orcid.org/0000-0002-7613-4617

Fernando R. Elorriaga-Verplancken1  * 
http://orcid.org/0000-0002-7360-8039

1Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, 23096 La Paz, Baja California Sur, Mexico.

2Departamento de Oceanología Biológica, Centro de Investigación Científica y de Educación Superior de Ensenada, 22860 Ensenada, Baja California, Mexico.


Abstract.

Over several decades, air temperature and sea surface temperature (SST) have increased in the northeastern Pacific, as has the frequency of large-scale warm anomalies in SST. The objective of this study was to evaluate the impact of these warm anomalies on the production of northern elephant seal (Mirounga angustirostris; NES) pups from the colony of the San Benito Archipelago, located in the central-western region of the Baja California Peninsula. Pup and adult female counts from the 2002 to 2019 breeding seasons were compiled to determine the trend in the abundance of the colony and its current state. In addition, birth rate variations during the study period were assessed. Likewise, the presence of warm anomaly events in the SST in the potential foraging area of adult females (PFA) was analyzed. The San Benito colony decreased at an average annual rate of 3.6% from 2002 to 2019, with an estimated abundance of 4,723 individuals (95% CI: 3,821-5,615) in 2019. However, the birth rate remained constant (mean 0.68 ± 0.08), even though several warm anomaly events associated with El Niño and The Blob phenomena were detected in the PFA. Our results suggest that large-scale warm anomalies in the SST do not severely impact NES pup production, thus the decline of the San Benito colony since the late 1900s could be due to other environmental factors, such as the increase in air temperature associated with climate change.

Key words: climate change; pinnipeds; population trend; pup production; sea surface temperature anomalies

Resumen.

Desde hace varias décadas, tanto la temperatura del aire como la temperatura superficial del mar (TSM) han incrementado en el Pacífico Nororiental, al igual que la frecuencia de anomalías cálidas de gran escala en la TSM. El objetivo del presente estudio fue evaluar el impacto de estas anomalías cálidas en la producción de crías de elefante marino del norte (Mirounga angustirostris; EMN) de la colonia del archipiélago San Benito, ubicada en la región centro-occidental de la península de Baja California. Se compilaron los conteos de crías y hembras adultas de las temporadas reproductivas de 2002 a 2019 para determinar la tendencia y la abundancia actual de la colonia, así como para evaluar las variaciones en la tasa de nacimientos durante el periodo de estudio. Asimismo, se analizó la presencia de eventos de anomalías cálidas en la TSM en la zona potencial de alimentación de las hembras adultas (ZPA). La colonia de San Benito decreció a una tasa anual promedio de 3.6% de 2002 a 2019, y para 2019 se estimó la abundancia en 4,723 individuos (IC 95%: 3,821-5,615). Sin embargo, la tasa de nacimientos se mantuvo constante (media 0.68 ± 0.08), a pesar de que se detectaron varios eventos de anomalías cálidas asociadas a los fenómenos de El Niño y La Mancha. Nuestros resultados sugieren que las anomalías cálidas de gran escala en la TSM no impactaron severamente la producción de crías del EMN, por lo que el declive de la colonia de San Benito desde finales de la década de 1990 podría deberse a otros factores ambientales, como el incremento en la temperatura del aire asociado al cambio climático.

Palabras clave: cambio climático; pinnípedos; tendencia poblacional; producción de crías; anomalías de temperatura superficial del mar

INTRODUCTION

Marine mammals are sentinel species that allow monitoring changes in the structure and function of marine ecosystems due to their conspicuous nature, longevity, fat reserves, and high trophic position (Bossart 2006, Hazen et al. 2019). They incorporate and reflect long-term spatial and temporal scale variations (Moore 2008) and reveal the response of ecosystems to environmental variability (Hazen et al. 2019). Within this group are the pinnipeds, which respond rapidly to changes in prey availability due to climatic oscillations (Le Boeuf and Crocker 2005, Robinson et al. 2012, Páez-Rosas et al. 2020).

The northern elephant seal (Mirounga angustirostris; NES) is distributed in the northeastern Pacific with breeding and haul-out sites located on islands and some continental beaches of Baja California, Mexico, and California, USA (Le Boeuf and Laws 1994). During their annual cycle, adults of both sexes migrate twice from breeding colonies to their main foraging areas located in high-latitude coastal and oceanic waters of the northeastern Pacific (Le Boeuf et al. 2000). The first migration (post-breeding migration) occurs at the end of the breeding season in winter (December-February), and the second (post-molt migration) after molting, which occurs in spring for females and in summer for males (Le Boeuf et al. 2000, Hückstädt 2015). During both migrations, females forage in areas between 40° and 45° N, but their longitudinal movements vary; females remain east of 160° W in the post-breeding migration, whereas, in the post-molting migration, they travel near 180° E (Robinson et al. 2012). In contrast, both male migrations are similar; they reach the Gulf of Alaska and the Aleutian Islands (Stewart and DeLong 1995, Le Boeuf et al. 2000).

During the last decade, large-scale oceanographic events impacted marine environments where NES forage. Since the early 2000s, there have been several El Niño events, which is the warm phase of the climatic and oceanographic phenomenon of El Niño/Southern Oscillation (ENSO), and the 2015-2016 event is one of the strongest on record (Kintisch 2016, L’Heureux 2016). In addition, from late 2013 to mid-2016, the marine heatwave called The Blob developed in the northeastern Pacific, with positive anomalies of up to 4 °C in the sea surface temperature (SST; Kintisch 2015, Peterson et al. 2016). The Blob originated in the southern Gulf of Alaska, extended to the west coast of the Baja California Peninsula, and reached an amplitude of around 2,000 km and 100 m depth (Bond et al. 2015, Kintisch 2015, Peterson et al. 2016). The combination of El Niño and The Blob produced unusual conditions in the northeastern Pacific (Bond et al. 2015, Cavole et al. 2016, Gentenmann et al. 2016): anomalously low chlorophyll a concentrations reflected by low primary productivity, tropical and subtropical species found in mid-latitudes, and increased frequency and intensity of harmful algal blooms (Cavole et al. 2016). As a result of these changes, there were mass mortality events of seabirds and marine mammals (Leising et al. 2015, Cavole et al. 2016, Gentenmann et al. 2016). By the summer of 2019, another marine heatwave referred to as The Blob 2.0 was recorded in the Gulf of Alaska, which had SST anomalies up to 2.5 °C above average (Amaya et al. 2020).

The effect of warm SST anomalies on the body condition of NES females and on pup production has been widely documented in California colonies (Le Boeuf and Crocker 2005, Crocker et al. 2006, Robinson et al. 2012). During strong El Niño events, the weight gain of females from the Año Nuevo colony in northern California has decreased due to an increased foraging effort. That is, females spend more time searching for prey patches but reduced periods on them, decreasing their foraging success compared to “normal” years (Crocker et al. 2006). Changes in the foraging strategy and a depleted female body condition appear not to severely impact the birth rate in the Año Nuevo colony (Le Boeuf and Reiter 1991, Crocker et al. 2006, Robinson et al. 2012). However, the weaning weight of pups born during or after El Niño years is lower, which may decrease the probability of juvenile survival (Le Boeuf and Crocker 2005).

Currently, there are 5 breeding colonies in Baja California (García-Aguilar et al. 2018). The main colonies are those of Guadalupe Island and San Benito Archipelago (Arias-del-Razo et al. 2017). The population size in Baja California for 2009 was estimated at 22,300 individuals (range: 18,600-26,000); however, numbers had declined at an average annual rate of 0.7% between 1970-2009 (García-Aguilar et al. 2018). To date, no information exists on the magnitude of the impact of warm SST events on the NES population of Baja California. Thus, in this paper, we analyze the pup production and birth rate of the San Benito colony over the last 2 decades, a period in which several events of large-scale warm SST anomalies occurred in the northeastern Pacific.

MATERIALS AND METHODS

Study area and data collection

The San Benito Archipelago is composed of 3 volcanic islands, namely East, Middle, and West, and a group of islets (Fig. 1). The archipelago, which is part of the Baja California Pacific Islands Biosphere Reserve, is located in the Pacific off Mexico (28°18ʹ N, 115°32ʹ W), 31.5 km west of Cedros Island and 130.0 km from the Baja California Peninsula. The climate is arid with an average annual rainfall of 65.1 to 121.3 mm, and the most amount of rain falls between December through February. The average annual air temperature varies between 19 to 20 °C (Junak and Philbrick 1999).

Figure 1 Location of the San Benito Archipelago, Baja California, Mexico. 

NES aggregate on all 3 islands during the breeding season in winter, but since there is a constant exchange of seals between the 3 islands (García-Aguilar 2005), we considered San Benito as a single reproductive unit, so the analyses were done at the colony level, not at the island level. Births occur from early December to early February (García-Aguilar 2004), and lactation lasts about 27 days (Le Boeuf 1972).

We compiled published and unpublished counts of live pups (suckling and weaned) and adult females for the period 2002-2019 (Table 1). Since pups remain on land up to ~2.5 months of age (Reiter et al. 1978), counts of this age class were carried out after the end of the birth season, assuming that all living pups were detected during counts. On the other hand, since NES females are asynchronous, they are not simultaneously found on land at any time during the breeding season; therefore, they cannot be counted in a single survey. The temporal distribution of females in the San Benito colony was described by García-Aguilar (2004) using the Rothery and McCann (1987) model, which allowed us to obtain correction factors based on the count date to estimate the total number of females that arrived each season to the colony (Table 1).

Table 1 Counts of northern elephant seal pups and adult female in the San Benito Archipelago, 2002-2019, and total number of adult females estimated based on correction factors. 

Pups Adult females
Season Date Count Date Count Correction factor Total
2001-2002 February 16-18, 2002a 2,024 January 19-25, 2002a 2,944 0.795 2,341
2002-2003 February 17-20, 2003a 2,050 January 18-21, 2003a 3,009 0.808 2,430
2003-2004 February 8-10, 2004b 1,771 January 15-18, 2004b 3,016 0.791 2,387
2008-2009 January 22-24, 2009c 1,689 January 22-24, 2009c 2,352 0.792 1,862
2012-2013 February 8-12, 2013d 1,504 February 8-12, 2013d 2,061 0.315 650
2013-2014 February 6-11, 2014d 1,097 February 6-11, 2014d 1,907 0.361 688
2014-2015 February 18-20, 2015d 1,205 February 18-20, 2015d 1,964 0.140 275
2016-2016 February 12-15, 2016e 1,317 February 12-15, 2016e 1,579 0.283 447
2018-2019 February 13-14, 2019 1,114 February 13-14, 2019 1,713 0.278 476

a García-Aguilar (2005), bGarcía-Aguilar (unpublished data), cFranco-Ortiz (2012), dElorriaga-Verplancken et al. (2015), eElorriaga-Verplancken and García-Aguilar (2018).

Colony trend and birth rate

The instantaneous rate of change (r) was obtained through a linear regression, in which the natural logarithm (ln) of the number of animals was the dependent variable and the time (years) was the independent variable. The annual rate of increase was calculated as λ = e r , where r is the slope of the linear regression (Caughley 1977). An analysis of variance (ANOVA) was performed to test the null hypothesis r = 0. The average annual rate of increase was obtained as (λ - 1) × 100 and expressed as a percentage. This analysis was performed separately for adult females and for pups.

The colony size was estimated for 2019 multiplying the number of pups produced by the factor M calculated for the NES population in California (Lowry et al. 2014), which reflects the population:pup ratio and varies according to λpups.

The birth rate, which represents the proportion of adult females that give birth in a single year (Croxall and Hiby 1983), was calculated for each season dividing the number of pups produced by the total number of adult females. A Z-test was performed to analyze variations in the birth rate over the study period.

Sea surface temperature anomalies

The potential foraging area for NES adult females of the San Benito colony, delimited by Aurioles et al. (2006) based on stable isotope analyses, is located ~8° south of those in California, between 31° and 43° N, and 126° to 175° W (Fig. 2). Monthly SST values with a 1-degree spatial resolution within this polygon were downloaded from the climate data library of the International Research Institute for Climate and Society (http://iridl.ldeo.columbia.edu/SOURCES/.NOAA, accessed 2022 September 01) for the period 1986-2020. Since SST trends are positive across the global ocean (L’Heureux et al. 2013), we first analyzed the trend in our study area. Quarterly average values (December-January-February, January-February-March, and so on) were calculated, which in turn were averaged to obtain annual estimates. The trend for SST for the period 1986-2020 was determined using the Mann-Kendall test (MK test) at a significant level of 0.05.

Figure 2 Potential foraging area (PFA) of northern elephant seal adult females of the San Benito colony (SBA). Based on Aurioles-Gamboa et al. (2006)

Given that the SST had a positive and significant trend in the study area (see below), we calculated the monthly anomalies for the period 2001-2019 following the methodology of the Climate Prediction Center for the Oceanic Niño Index (http://cpc.ncep.noaa.gov, accessed 2022 September 10), which consists of using 30-year base periods to detect anomalies in successive periods of 5 years. Thus, for the years 2001-2004 we used the base period 1986-2015; for 2005-2009, the base period 1991-2020. However, for the last two 5-year periods (2010-2014 and 2015-2019), since the time series corresponding to the base periods 1996-2025 and 2001-2030 are not complete, we used the base period 1991-2020.

RESULTS

Between 2002 and 2019, the number of pups and adult females decreased, with average annual rates of 3.58% and 3.78%, respectively (Table 2, Fig. 3). Since λpups = 0.964, the colony size for 2019 was estimated by multiplying the number of pups produced in that year by 4.24 (the multiplicative factor M). Thus, an abundance of 4,723 individuals (95% CI: 3,821-5,615) was estimated. The West Island congregated the largest number of seals (56% of the total), followed by the Middle (33%) and East (11%) islands.

Table 2 Average annual rate of increase (λ) of pups and adult females of northern elephant seals in the San Benito Archipelago, 2002-2019. N = number of counts, r = instantaneous rate of change, R2 = coefficient of determination. 

N r R2 λ
Pups 9 -0.036 0.87 0.964
Adult females 9 -0.039 0.94 0.962

Figure 3 Number of northern elephant seal pups and females in the San Benito colony in 2002-2019. 

The birth rate remained stable throughout the study period, with a mean of 0.68 ± 0.08, varying from 0.58 in 2014 to 0.83 in 2016 (Fig. 4). Z-scores were not significant (P > 0.05), except for the 2016 season, which was slightly above average (Z = 1.96, P = 0.049).

Figure 4 Estimated birth rate of the northern elephant seal in the San Benito colony in 2002-2019. 

The MK test revealed positive and significant SST trends in the potential foraging area of San Benito females for the period 1986-2020 (Z = 3.18, P < 0.01; Fig. 5), with a mean increment of 0.18 °C per decade. SST anomalies revealed that 2003, 2006-2007, 2009-2010, and 2016 were years in which cold conditions (SST anomaly less than or equal to -0.25 °C) prevailed, whereas in 2001, 2004, 2008-2009, 2011-2015, and 2019 warm conditions (SST anomaly ≥ 0.25 °C) predominated (Fig. 6).

Figure 5 Mean annual sea surface temperature (SST; 1986-2020) in the potential foraging area of northern elephant seal adult females from the San Benito colony. 

Figure 6 Monthly anomaly (January 2001-December 2019) of the sea surface temperature (SST) in the potential foraging area of northern elephant seal adult females from the San Benito colony. 

DISCUSSION

The reproductive success of a species is strongly related with the success of its foraging strategies, which can be affected by anomalous environmental conditions (Crocker et al. 2006). NES females consume wide-ranging epi- and mesopelagic prey (Riofrío-Lazo et al. 2012), mainly squid and myctophid fish (Antonelis et al. 1994, Goetsch 2018), and environmental stress conditions could impact their foraging success, which may reduce pup production. Nevertheless, our results suggest that, as observed in the Año Nuevo colony, this was not the case for females from the San Benito colony. However, there is a sustained negative trend in pup production since the late 1990s (García-Aguilar et al. 2018, present study), which appears to be unrelated to the presence of large-scale events of warm SST anomalies, in contrast to what has been observed for other pinnipeds from the California Current ecosystem, such as the California sea lion (Zalophus californianus) or the Guadalupe fur seal (Arctocephalus townsendi) (Elorriaga-Verplancken et al. 2016, Delong et al. 2017). In fact, the stable NES birth rates observed in our study period (2002-2019) indicate that there was no impact despite the occurrence of several El Niño events and The Blob.

The persistent decrease of the San Benito colony, like that observed in the Guadalupe Island colony, could be due to the movements of seals towards the colonies in southern California in response to the sustained increase in air temperature in the region, as proposed by García-Aguilar et al. (2018). The fact that both the number of adult females and the number of pups has decreased at a similar average annual rate (~3.6%) during the last 2 decades with a birth rate that has not declined, suggests that the reproductive success of females (expressed exclusively in terms of pup production) has been constant over this period. Therefore, the negative trend could be explained by the proposed migration to the north. Nevertheless, further research is needed to expand our knowledge on this regard.

How the distribution of animals in the San Benito Archipelago has changed over time is noteworthy. East Island was apparently the first to be occupied in the late 1910s, and for several decades the largest number of NES congregated there (Williams 1941). By the mid-1960s, animals were observed moving to the West and Middle islands (Rice et al. 1965). In the early 2000s, the largest number of animals congregated on the Middle Island, followed by the West Island and East Island (García-Aguilar 2005). The recent distribution is different: in 2019 most of the NES congregated on the West Island. The gradual abandonment of the Middle Island in recent years could be associated with increasingly frequent heatwaves (i.e., days with an average maximum air temperature >25 °C) during winter and spring (García-Aguilar et al. 2018) that severely impact pup survival in harems without access to the sea (Salogni et al. 2016), which were common 20 years ago but now no longer exist.

Two non-exclusive explications were proposed regarding why birth rates are not severely impacted by large-scale warm anomaly events (Crocker et al. 2006). The first concerns the foraging strategy of NES females, which forage for prolonged periods in deep (up to ~700 m) oceanic waters, where the effect of these events is weaker than in coastal waters. The second explanation concerns the lagged effect of warm anomalies along the food web, hence the lagged impact on top predators. Considering these 2 explanations, it is unsurprising that the reduction observed in the birth rate was not drastic in the San Benito colony during the strong El Niño event of 2015-2016 or The Blob in 2013-2016. In fact, stable isotope (δ15N and δ13C) analyses showed that NES females from the San Benito colony did not change their habitat use throughout these events, except towards the end of the 2014 and 2018 post-molting migration, when they apparently expanded their foraging range (Rodríguez-Rafael 2021).

Our results confirm the persistent decline of the San Benito colony since the end of the 20th century. However, there was no evidence that this decline was caused by a decrease in female reproductive success associated with anomalous warming events in the northeast Pacific. Instead, the results support the scenario in which animals are migrating from colonies of Baja California to colonies of California. These types of assessments must continue over time, complemented by additional approaches such as stable isotope analyses or telemetry, to strengthen our knowledge of how NES use marine and terrestrial habitats, especially given the recent increase in the frequency of warm anomalies in the Pacific Ocean (Freund et al. 2019) and the positive trend in air temperature in the region (Cayan et al. 2008).

This study provides information exclusively on the current status of the San Benito NES colony. However, the present study is part of the comprehensive effort of different Mexican academic institutions to understand the ecological processes that determine the population dynamics of this and other pinniped species that inhabit the Baja California Pacific Islands Biosphere Reserve, such as the California sea lion, the Guadalupe fur seal, and the Pacific harbor seal (Phoca vitulina). The conjunction of the information generated is an essential tool to create a program aimed at the management and conservation of these species in the region.

Conflict of interest

The authors state that there is no conflict of interest.

ACKNOWLEDGMENTS

This study was financially supported by the Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCYT, Mexico, grant number CB-181876) and Proyectos Internos of the Instituto Politécnico Nacional (20130944, 20140277, 20150326, 20160164, 20170526, and 20181645, 20195860). FREV and FGM thank the Instituto Politécnico Nacional for the scholarships (COFAA and EDI). EDRR thanks to Instituto Politécnico Nacional and CONAHCYT for the BEIFI and Posgrado Nacional scholarships, respectively. Likewise, we are grateful to the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT, Mexico) for the research permits SGPA/DGVS/11309/12, 11744/13, 00195/15, 00050/16, 00091/17, 002460/18 and /01643/19 granted through the Dirección General de Vida Silvestre. We thank the Cooperativa Pesquera “Pescadores Nacionales de Abulón” of Cedros Island for their support in the field.

REFERENCES

Amaya, DJ, Miller, AJ, Xie, SP, Kosaka, Y. 2020. Physical drivers of the summer 2019 North Pacific marine heatwave. Nat Commun. 11:1903. https://doi.org/10.1038/s41467-020-15820-w [ Links ]

Antonelis, GA, Lowry, MS, Fiscus, CH, Stewart, BS, DeLong, RL. 1994. Diet of the northern elephant seal. In: Le-Boeuf, BJ, Laws, RM (eds.), Elephant Seals: Population Ecology, Behavior, and Physiology. Berkeley (CA): University of California Press. p. 211-223. [ Links ]

Arias-Del-Razo, A, Schramm, Y, Heckel, G, Milanés-Salinas, Á, García-Capitanachi B, Lubinsky-Jinich D. 2017. Distribution of four pinnipeds (Zalophus californianus, Arctocephalus philippii townsendi, Phoca vitulina richardii, and Mirounga angustirostris) on islands off the west coast of the Baja California Peninsula, Mexico. Aquat Mamm. 43(1):40-51. https://doi.org/10.1578/AM.43.1.2017.40 [ Links ]

Aurioles, D, Koch, PL, Le Boeuf, BJ. 2006. Differences in foraging location of Mexican and California elephant seals: evidence from stable isotopes in pups. Mar Mam Sci. 22(2):326-338. https://doi.org/10.1111/j.1748-7692.2006.00023.x [ Links ]

Bond, NA, Cronin, MF, Freeland, H, Mantua, N. 2015. Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys Res Lett. 42(9):3414-3420. https://doi.org/10.1002/2015GL063306 [ Links ]

Bossart, GD. 2006. Marine mammals as sentinel species for oceans and human health. Ocean. 19(2):134-137. https://doi.org/10.5670/oceanog.2006.77 [ Links ]

Caughley, G. 1977. Analysis of Vertebrate Populations. London: John Wiley & Sons, Inc. 244 p. [ Links ]

Cavole, LM, Demko, AM, Diner, RE, Giddings, A, Koester, I, Pagniello, CMLS, Paulsen, ML, Ramirez-Valdez, A, Schwenck, SM, Yen, NK, et al. 2016. Biological impacts of the 2013-2015 warm-water anomaly in the Northeast Pacific: Winners, losers, and the future. Ocean. 29(2):273-285. http://doi.org/10.5670/oceanog.2016.32 [ Links ]

Cayan, DR, Maurer EP, Dettinger MD, Tyree M, Hayhoe K. 2008. Climate change scenarios for the California region. Clim Change 87(1):21-42. http://doi.org/10.1007/s10584-007-9377-6 [ Links ]

Crocker, DE, Costa, DP, Le Boeuf, BJ, Webb, PM, Houser, DS. 2006. Impact of El Niño on the foraging behavior of female northern elephant seals. Mar Ecol Prog Ser. 309:1-10. http://doi.org/10.3354/meps309001 [ Links ]

Croxall, JP, Hiby, L. 1983. Fecundity, survival and site fidelity in Weddell seals, Leptonychotes weddelli. J Appl Ecol. 20(1):19-32. https://doi.org/10.2307/2403373 [ Links ]

DeLong, RL, Melin, SR, Laake, JL, Morris, P, Orr, AJ, Harris, JD. 2017. Age- and sex-specific survival of California sea lions (Zalophus californianus) at San Miguel Island, California. Mar Mammal Sci. 33(4):1097-1125. https://doi.org/10.1111/mms.12427 [ Links ]

Elorriaga-Verplancken, FR, Ferretto, G, Angell, OC. 2015. Current status of the California sea lion (Zalophus californianus) and the northern elephant seal (Mirounga angustirostris) at the San Benito Archipelago, Mexico = Estado actual del lobo marino de California (Zalophus californianus) y el elefante marino del norte (Mirounga angustirostris) en el archipiélago San Benito, México. Cienc Mar. 41(4):269-281. http://doi.org/10.7773/cm.v41i4.2545 [ Links ]

Elorriaga-Verplancken, FR, García-Aguilar, MC. 2018. Interannual (2002-2016) variation in the natality rate of the northern elephant seal (Mirounga angustirostris) at the San Benito colony, Baja California, Mexico. Mar Mam Sci. 34(3):823-828.http://doi.org/10.1111/mms.12486 [ Links ]

Elorriaga-Verplancken, FR, Sierra-Rodríguez, GE, Rosales-Nanduca, H, Acevedo-Whitehouse, K, Sandoval-Sierra, J. 2016. Impact of the 2015 El Niño-Southern Oscillation on the abundance and foraging habits of Guadalupe fur seals and California sea lions from the San Benito Archipelago, Mexico. PLoS One. 11(5):e0155034. http://doi.org/10.1371/journal.pone.0155034 [ Links ]

Franco-Ortiz, M. 2012. Distribución y abundancia del elefante marino del norte, Mirounga angustirostris, en México [Distribution and abundance of the northern elephant seal, Mirounga angustirostris, in Mexico ] [MSc thesis]. [Ensenada, (Mexico)]: Universidad Autónoma de Baja California. 209 p. [ Links ]

Freund, MB, Henley, BJ, Karoly, DJ, McGregor, HV, Abram, NJ, Dommenget, D. 2019. Higher frequency of Central Pacific El Niño events in recent decades relative to past centuries. Nat Geosci. 12:450-455. https://doi.org/10.1038/s41561-019-0353-3 [ Links ]

García-Aguilar, MC. 2004. Breeding biology of the northern elephant seal (Mirounga angustirostris) at the Isla San Benito del Oeste, Eastern Pacific, Mexico. Aquat Mamm. 30(2):289-295. http://doi.org/10.1578/AM.30.2.2004.289 [ Links ]

García-Aguilar, MC. 2005. Demografía y ecología de la conducta del elefante marino del norte (Mirounga angustirostris) en las islas San Benito, México. [Demography and behavioral ecology of the northern elephant seal (Mirunga angustirostris) in the San Benito Islands, Mexico] [dissertation]. [Ensenada (Mexico)]: Centro de Investigación Científica y de Educación Superior de Ensenada. 147 p. [ Links ]

García-Aguilar, MC, Turrent, C, Elorriaga-Verplancken, FR, Arias-Del-Razo, A, Schramm, Y. 2018. Climate change and the northern elephant seal (Mirounga angustirostris) population in Baja California, Mexico. PLoS One. 13(2):ee0193211. https://doi.org/10.1371/journal.pone.0193211 [ Links ]

Gentenmann, CL, Fewings, MR, García-Reyes, M. 2016. Satellite sea surface temperatures along the west coast of the United States during the 2014-2016 northeast pacific marine heat wave. Geophys Res Lett. 44(1):312-319. http://doi.org/10.1002/2016GL071039 [ Links ]

Goetsch, C. 2018. Illuminating the twilight zone: diet and foraging strategies of a deep-sea predator, the northern elephant seal [dissertation]. [Santa Cruz (CA)]: University of California Santa Cruz. 207 p. [ Links ]

Hazen, EL, Abrahms, B, Brodie, S, Carroll, G, Jacox, MG, Savoca, MS, Scales, KL, Sydeman, WJ, Bograd, SJ. 2019. Marine top predators as climate and ecosystem sentinels. Front Ecol Environ. 17(10):565-574. http://doi.org/10.1002/fee.2125 [ Links ]

Hückstädt, L. 2015. Mirounga angustirostris. The IUCN Red List of Threatened Species 2015:e.T13581A45227116. http://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T13581A45227116.enLinks ]

Junak, SA, Philbrick, R. 1999. Flowering plants of the San Benito Islands, Baja California, Mexico. In: Browne, DR, Mitchell, KL, Chaney, HW (eds.), Proceedings of the 5th California Islands Symposium; 29 Mar-1 Apr 1999, vol. 1. Santa Barbara (CA): Santa Barbara Museum of the Natural History. p. 235-246. [ Links ]

Kintisch, E. 2015. “The Blob” invades Pacific, flummoxing climate experts. Science. 348(6230):17-18. http://doi.org/10.1126/science.348.6230.17 [ Links ]

Kintisch, E. 2016. How a “Godzilla” El Niño shook up weather forecasts. Science. 352(6293):1501-1502. http://doi.org/10.1126/science.352.6293.1501 [ Links ]

L’Heureux, M. 2016. The 2015-16 El Niño. In: NOAA’s National Weather Service (eds.), 41st NOAA Annual Climate Diagnostics and Prediction Workshop; 03-06 Oct 2016. Orono (ME, USA): [NWS] National Weather Service. p. 4-7. https://doi.org/10.7289/v5js9nh0 [ Links ]

L’Heureux, ML, Lee, S, Lyon, B. 2013. Recent multidecadal strengthening of the Walker circulation across the tropical Pacific. Nat Clim Change. 3:571-576. http://doi.org/10.1038/nclimate1840 [ Links ]

Le Boeuf, BJ. 1972. Sexual behavior in the northern elephant seal Mirounga angustirostris. Behaviour. 41(1):1-26. http://doi.org/10.1163/156853972x00167 [ Links ]

Le Boeuf, BJ, Crocker, DE. 2005. Ocean climate and seal condition. BMC Biol. 3:9. https://doi.org/10.1186/1741-7007-3-9 [ Links ]

Le Boeuf, BJ, Crocker, DE, Costa, DP, Blackwell, SB, Webb, PM, Houser, DS. 2000. Foraging ecology of northern elephant seals. Ecol Monogr. 70(3):353-382. https://doi.org/10.2307/2657207 [ Links ]

Le Boeuf, BJ, Laws, RM. 1994. Elephant seals: An introduction to the genus. In: Le Boeuf, BJ, Laws, RM (eds.), Elephant Seals: Population Ecology, Behavior, and Physiology. Berkeley (CA): University of California Press. p. 1-26. [ Links ]

Le Boeuf, BJ, Reiter, J. 1991. Biological effects associated with El Niño, Southern Oscillation 1982-83, on northern elephant seals breeding at Año Nuevo, California. In: Trillmich, F, Ono, KA (eds.), Pinnipeds and El Niño: Responses to Environmental Stress. New York (NY): Springer-Verlag. p. 206-218. [ Links ]

Leising, AW, Schroeder, ID, Bograd, SJ, Abell, J, Durazo, R, Gaxiola-Castro, G, Bjorkstedt, EP, Field, J, Sakuma, K, Robertson, RR, et al. 2015. State of the California Current 2014-15: Impacts of the warm-water “Blob”. CalCOFI Rep. 56:31-68. [ Links ]

Lowry, MS, Condit, R, Hatfield, B, Allen, SG, Berger, R, Morris, PA, Le Boeuf, BJ, Reiter, J. 2014. Abundance, distribution, and population growth of the Northern Elephant Seal (Mirounga angustirostris) in the United States from 1991 to 2010. Aquat Mamm. 40(1):20-31. https://doi.org/10.1578/AM.40.1.2014.20 [ Links ]

Moore, SE. 2008. Marine mammals as ecosystem sentinels. J Mammal. 89(3):534-540. https://doi.org/10.1644/07-MAMM-S-312R1.1 [ Links ]

Páez-Rosas, D, Moreno-Sánchez, X, Tripp-Valdez, A, Elorriaga-Verplancken, FR, Carranco-Narváez, S. 2020. Changes in the Galapagos sea lion diet as a response to El Niño-Southern Oscillation. Reg Stud Mar Sci. 40:101485. https://doi.org/10.1016/j.rsma.2020.101485 [ Links ]

Peterson, W, Bond, N, Robert, M. 2016. The Blob (Part Three): Going, going, gone? PICES Press. 24(1):46-49. [ Links ]

Reiter, J, Stinson, NL, Le Boeuf, BJ. 1978. Northern elephant seal development: The transition from weaning to nutritional independence. Behav Ecol Sociobiol. 3(4):337-367. https://doi.org/10.1007/BF00303199 [ Links ]

Rice, DW, Kenyon, KW, Lluch-Blenda, D. 1965. Pinniped populations at Islas Guadalupe, San Benito, and Cedros, Baja California, in 1965. Trans San Diego Soc Nat Hist. 14:73-84. [ Links ]

Riofrío-Lazo, M, Aurioles-Gamboa, D, Le Boeuf, BJ. 2012. Ontogenetic changes in feeding habits of northern elephant seals revealed by δ15N and δ13C analysis of growth layers in teeth. Mar Ecol Prog Ser. 450:229-241. https://doi.org/10.3354/meps09562 [ Links ]

Robinson, PW, Costa, DP, Crocker, DE, Gallo-Reynoso, JP, Champagne, CD, Fowler, MA, Goetsch, C, Goetz, KT, Hassrick, JL, Hückstädt, LA, et al. 2012. Foraging behavior and success of a mesopelagic predator in the northeast Pacific Ocean: insights from a data-rich species, the northern elephant seal. PLoS ONE. 7:e36728. https://doi.org/10.1371/journal.pone.0036728 [ Links ]

Rodríguez-Rafael, ED. 2021. Caracterización isotópica y de abundancia de elefantes marinos del norte (Mirounga angustirostris) del Archipiélago San Benito, México, y su relación con anomalías ambientales del Pacífico Nororiental. [Isotopic and abundance characterization of northern elephant seals (Mirounga angustirostris) from the San Benito Archipelago, Mexico, and its relationship with environmental anomalies of the Northeast Pacific] [MSc thesis]. [La Paz (Mexico)]: Centro Interdisciplinario de Ciencias Marinas. 62 p. [ Links ]

Rothery, P, McCann, TS. 1987. Estimating pup production of elephant seals at South Georgia. In: Harris, S (ed.), Mammal population studies. The proceedings of a symposium held at the Zoological Society of London; 28-29 Nov 1986. vol. 58. Oxford (UK): Zoological Society of London. p. 211-223. [ Links ]

Salogni, E, Sanvito, S, Galimberti, F. 2016. Postmortem examination and causes of death of northern elephant seal (Mirounga angustirostris) pups of the San Benito Islands, Baja California, Mexico. Mar Mam Sci. 32(2):743-752. https://doi.org/10.1111/mms.12273 [ Links ]

Stewart, BS, DeLong, RL. 1995. Double migrations of the northern elephant seal, Mirounga angustirostris. J Mammal. 76(1):196-205. https://doi.org/10.2307/1382328 [ Links ]

Williams, W. 1941. Jumbo of the deep. Nat Hist. 48:145-149. [ Links ]

Received: May 16, 2022; Accepted: April 10, 2023

*Corresponding author. E-mail: felorriaga@ipn.mx

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License