Environment‐sensitive mass changes influence breeding frequency in a capital breeding marine top predator

Abstract

The trade‐off between survival and reproduction in resource‐limited iteroparous animals can result in some individuals missing some breeding opportunities. In practice, even with the best observation regimes, deciding whether ‘missed’ years represent real pauses in breeding or failures to detect breeding can be difficult, posing problems for the estimation of individual reproductive output and overall population fecundity. We corrected fecundity estimates by determining whether breeding had occurred in skipped years, using long‐term capture–recapture observation datasets with parallel longitudinal mass measurements, based on informative underlying relationships between individuals’ mass, breeding status and environmental drivers in a capital breeding phocid, the grey seal. Bayesian modelling considered interacting processes jointly: temporal changes in a phenotypic covariate (mass); relationship of mass to breeding probability; effects of maternal breeding state and mark type on resighting. Full reproductive histories were imputed, with the status of unobserved animals estimated as breeding or non‐breeding, accounting for local environmental variation. Overall fecundity was then derived for Scottish breeding colonies with contrasting pup production trends. Maternal mass affected breeding likelihood. Mothers with low body mass at the end of breeding were less likely to bear a pup the following year. Successive breeding episodes incurred a cost in reduced body mass which was more pronounced for North Rona, Outer Hebrides (NR) mothers. Skipping breeding increased subsequent pupping probability substantially for low mass females. Poor environmental conditions were associated with declines in breeding probability at both colonies. Seal mass gain between breeding seasons was (a) negatively associated with lagged North Atlantic Oscillation for seals at NR and (b) positively associated with an index of seal prey (Ammodytes spp) abundance at Isle of May, Firth of Forth (IM). Overall fecundity was marginally greater at IM (increasing/stable pup production) than at NR (decreasing). No effects of mass were detected on maternal survival. Skipping breeding in female grey seals appears to be an individual mass‐dependent constraint moderated by previous reproductive output and local environmental conditions. Different demographic trends at breeding colonies were consistent with the fecundities estimated using this method, which is general and adaptable to other situations.

Modeling Recruitment of Birth Cohorts to the Breeding Population: A Hidden Markov Model Approach

“…The remaining two could be relaxed through the inclusion of temporary migration. Temporary migration would permit individuals to skip breeding seasons, which is known to happen (Smout et al, 2020), or to temporarily breed at a different colony. The consequence of not incorporating this into the model is that capture probabilities are likely to underestimate the true values and as a result there may be modest effects on the estimation of recruitment.…”

“…For example, an individual with capture history 1 0 0 1 1 was initially captured and marked as a pup, missed on the following two occasions (indicated by the zeros) before being resighted on the final two occasions. Resighted seals were assumed to be breeding; resight probabilities for non-breeding seals are known to be very small (Smout et al, 2020). The observed data that we will analyse consist of the capture histories for female seals tagged as pups in 1991-1994 that have been recaptured as breeding adults on the Isle of May at least once during the 1992-2011 breeding seasons.…”

Energetic limits: Defining the bounds and trade‐offs of successful energy management in a capital breeder

“…This pattern was seen regardless of individual differences in background energy expenditures (Figure 4). Previous work has demonstrated that female seals may adjust their reproductive output between years, when faced with changing environmental conditions prior to the lactation period, in order to maximize lifetime reproductive output (Bowen et al, 2015; Desprez et al., 2018; Kalberer, Meise, Trillmich, & Krüger, 2018; McMahon et al., 2016; Pomeroy et al., 1999; Smout et al., 2020), but research has yet to reveal the mechanism for terminating lactation in grey seals (e.g. by investigating metabolite trends leading up to weaning; Mellish & Iverson, 2001; Watson, Pomeroy, Al‐Tannak, & Kennedy, 2020).…”

“…Throughout each breeding season, researchers surveyed the main breeding areas daily so that known seals were identified as soon as possible after coming ashore (Smout, King, & Pomeroy, 2020). When birth was not observed directly, it was estimated using age‐related mass and development characteristics (Kovacs & Lavigne, 1986).…”

Reactive stress-coping styles show more variable reproductive expenditure and fitness outcomes

“…From late October to early December, individual females spend 18-20 days on the island, during which time they each bear and nurse one pup, enter oestrus approximately 16 days post-parturition 62 , mate, and abruptly wean their pup around day 18 of lactation 41 . The Isle of May colony was part of a long-term study of grey seal reproductive energetics and behaviour by the Sea Mammal Research Unit, SMRU 41,63 . Known individuals can be identified using pre-existing brands, flipper tags and/or pelage patterns 41,64 .…”