OldClimateEcosystem.Rmd

---
title: "Old Climate Ecosystem"
author: "Sarah Gaichas"
date: "`r Sys.Date()`"
output: html_document
---

```{r setup, include=FALSE}
knitr::opts_chunk$set(echo = TRUE)
```

### Climate Change Indicators: ocean temperatures, extreme events, currents, acidification

#### Ocean temperature and salinity
The ocean continues to warm, altering habitat conditions experienced by a wide range of species.  2022 was among the warmest years on record in the North Atlantic [@cheng_another_2023] and ocean temperatures continue to warm at both the surface (Fig. \ref{fig:seasonal-sst-anom-gridded}) and bottom (Fig. \ref{fig:bottom-temp}) throughout New England. Seasonal sea surface temperatures in 2022 were above average throughout the year, with some seasons rivaling or exceeding the record warm temperatures observed in 2012.

```{r seasonal-sst-anom-gridded, fig.cap="New England (EPUs outlined in grey) 2022 seasonal sea surface temperature (SST) anomalies. The anomalies are the difference between the 2022 seasonal means and the long-term (1991-2020) seasonal means.  Seasons are defined as: Jan-Mar for winter, Apr-Jun for spring, Jul-Sep for summer, and Oct-Dec for fall.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-seasonal-sst-anomaly-gridded.R"), fig.width = 7, fig.asp = .8}
```

```{r bottom-temp, fig.cap="Annual Georges Bank and Gulf of Maine seasonal bottom temperature anomalies. Data are obtained from GLORYS, a global ocean reanalysis product that provides high resolution data on ocean physics and incorporates real-time observations.  Data from the last two years (open circles) are from a near-real-time model (PSY) and are considered preliminary.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-seasonal-bt-anom.R"), fig.width=6}
```

In addition to increasing seasonal temperatures, ocean summer conditions now last longer within each year. In both GB and GOM, the transition date from cool winter conditions to warm stratified summer conditions is getting earlier. The transition back to well mixed cool temperatures is also getting later in the year, thus increasing the total number of days when the surface temperatures are in the warm summer conditions (Fig. \ref{fig:transition}).

```{r transition, fig.cap="Ocean summer length in New England: the annual total number of days between the spring thermal transition date and the fall thermal transition date.  The transition dates are defined as the day of the year when surface temperatures changeover from cool to warm conditions in the spring and back to cool conditions in the fall. The left is Georges Bank (GB) and the right is Gulf of Maine (GOM).", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-sumlength.R"), fig.width=6, fig.asp=0.3}

```

#### Extreme temperature events
The increase in surface and bottom water temperature observed in the Northeast US can cause long term incremental stress on marine organisms, especially those relying on cooler water habitats for some or all life stages. In addition to changes in long-term average conditions, short-term extreme temperature events can produce acute stress on marine organisms, especially when the baseline temperature is increasing. To identify these extreme events separately from the baseline warming, we have changed our methods to detect marine heatwaves (MHWs, [@hobday_hierarchical_2016; @jacox_thermal_2020; @jacox_global_2022]) to remove the global warming signal. Therefore, these indicators are different than in previous reports, but MHWs identified now are truly extreme departures from an already warming ecosystem.  A combination of long-term ocean warming and MHWs should be used to assess total heat stress on marine organisms.

In 2022, GB experienced one surface MHW that began on October 26^th^, peaked on November 7^th^ and lasted 28 days (Fig. \ref{fig:heatwave-year-gb}).  This surface MHW ranked 17^th^ on record in terms of maximum intensity and 5^th^ on record in terms of cumulative intensity.

```{r heatwave-year-gb, fig.cap="Marine heatwave events (red shading above black line) on Georges Bank occuring in 2022.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-heatwave-year-detrended_gb.R"), fig.asp=.65}
```

The GOM experienced four surface MHWs in 2022 that began on August 4^th^ and 25^th^, September 9^th^, and October 31^th^ (Fig \ref{fig:heatwave-year-gom}).  The strongest event in terms of maximum intensity began on August 4^th^ and peaked on August 7^th^ lasting six days.  This surface MHW ranked 27^th^ on record.  The five most intense surface MHW events on record in the GOM occurred over the last 12 years.  No bottom MHWs were detected for either GB or GOM in 2022.

```{r heatwave-year-gom, fig.cap="Marine heatwave events (red shading above black line) in the Gulf of Maine occuring in 2022.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-heatwave-year-detrended_gom.R"), fig.asp=.65}
```

#### Ocean currents and features

Variability of the Gulf Stream is one of the major drivers of changes in the oceanographic conditions of the Slope Sea and subsequently the Northeast U.S. continental shelf [@gangopadhyay_census_2020]. Changes in the Gulf Stream and Slope Sea can affect large-scale climate phenomena as well as local ecosystems and coastal communities. During the last decade, the Gulf Stream has become less stable and shifted northward [@andres_recent_2016; @caesar_observed_2018] (Fig. \ref{fig:GSI}).  A more northern Gulf Stream position is associated with warmer ocean temperature on the northeast shelf [@zhang_role_2007], a higher proportion of Warm Slope Water in the Northeast Channel, and increased sea surface height along the U.S. east coast [@goddard_extreme_2015].

```{r GSI, fig.cap = "Index representing changes in the location of the Gulf Stream north wall. Positive values represent a more northerly Gulf Stream position.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_MAB.Rmd-gsi.R"), fig.width=5, fig.asp = 0.4}
```

Since 2008, the Gulf Stream has moved closer to the Grand Banks, reducing the supply of cold, fresh, and oxygen-rich Labrador Current waters to the Northwest Atlantic Shelf [@goncalves_neto_changes_2021]. Nearly every year since 2010, warm slope water made up more than 75% of the annual slope water proportions entering the Gulf of Maine.  In 2017 and 2019, almost no cooler Labrador Slope water entered the Gulf of Maine through the Northeast Channel (Fig. \ref{fig:wsw-prop}).  The changing proportions of source water affect the temperature, salinity, and nutrient inputs to the Gulf of Maine ecosystem.  In 2021, warm slope water continued to dominate (86.1%) inputs to the Gulf of Maine. 

```{r wsw-prop, fig.cap = "Proportion of Warm Slope Water (WSW) and Labrador slope water (LSLW) entering the GOM through the Northeast Channel.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-slopewater.R"), fig.width=5.5, fig.asp=.4}
```

The increased instability of the Gulf Stream position and warming of the Slope Sea may also be connected to the regime shift increase in the number of warm core rings formed annually in the Northwest Atlantic [@gangopadhyay_observed_2019; @gangopadhyay_census_2020] (Fig. \ref{fig:wcr}). When warm core rings and eddies interact with the continental slope they can transport warm, salty water to the continental shelf [@chen_mesoscale_2022], which can alter the habitat and disrupt seasonal movement of fish [@gawarkiewicz_changing_2018].  The transport of offshore water onto the shelf is happening more frequently [@gawarkiewicz_changing_2018; @gawarkiewicz_increasing_nodate] and can contribute to extreme temperatures (i.e. marine heatwaves) along the continental shelf [@gawarkiewicz_characteristics_2019; @chen_mesoscale_2022] as well as the movement of shelf-break species inshore [@gawarkiewicz_changing_2018; @potter_horizontal_2011; @worm_predator_2003]. 


2022 had the same number of warm core rings (21) as 2021, but most of the 2022 rings formed east of 60 W and fewer were observed near the shelf break region.  Warm core rings near GB likely contributed to the marine heatwave and anomalously warm fall surface temperatures.

```{r wcr, fig.cap= "Warm core ring formation on the Northeast U.S. Shelf: Annual number of rings.  A significant regime shift is denoted by the split red line as noted in Gangopadhyay et al. 2019.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_MAB.Rmd-wcr.R")}

```

Changes in ocean temperature and circulation alter habitat features such as the seasonal cold pool, a 20–60 m thick band of cold, relatively uniform near-bottom water that persists from spring to fall over the mid and outer shelf of the Mid-Atlantic Bight and southern flank of GB [@lentz_seasonal_2017; @chen_seasonal_2018]. It is a reservoir of nutrients that feeds phytoplankton productivity, is essential fish spawning and nursery habitat, and affects fish distribution and behavior [@lentz_seasonal_2017; @miles_offshore_2021]. The average temperature of the cold pool is getting warmer over time [@miller_state-space_2016; @du_pontavice_incorporating_nodate], the area is getting smaller [@friedland_middle_2022], and the duration is getting shorter (Fig. \ref{fig:cold-pool}).

```{r cold-pool, fig.cap="Seasonal cold pool indices: mean temperature within the cold pool, cold pool persistence, and spatial extent.",  code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_MAB.Rmd-cold_pool.R"), fig.width=10, fig.asp=.3}

```

#### Ocean Acidification
Ocean acidification (OA) has caused measured declines in global ocean pH, and is projected to continue declining if high carbon dioxide emissions continue [@intergovernmental_panel_on_climate_change_ipcc_technical_2022]. OA also changes the availability of minerals required by organisms to form calcified structures such as shells and other structures. Calcifying conditions in seawater can be determined by measuring aragonite saturation state ($\Omega_{Arag}$), the tendency of a common type of calcium carbonate, aragonite, to form or dissolve.  When $\Omega_{Arag}$ is less than 1, shells and other calcium carbonate structures begin to dissolve. Typical surface ocean $\Omega_{Arag}$ is 2-4, but extremes can be <1 or >5 [@jiang_climatological_2015]. As the ocean absorbs carbon dioxide, both pH and $\Omega_{Arag}$ decrease and can cause organisms to respond with reduced survival, calcification rates, growth, and reproduction, as well as impaired development, and/or changes in energy allocation [@kroeker_impacts_2013 @saba_recommended_2019]. However, sensitivity levels vary, and some organisms exhibit negative responses to calcification and other processes when $\Omega_{Arag}$ is as low as 3.

Summer-time (2007-present) $\Omega_{Arag}$ on the U.S. Northeast Shelf varies in space and time, ranging from 0.64 to 2.49 (Fig. \ref{fig:ne-oa}, left panel). Spatially, the lowest bottom $\Omega_{Arag}$ has occurred in the Gulf of Maine, western Long Island Sound, nearshore to mid-shelf waters of the Mid-Atlantic Bight off the coast of New Jersey, and in waters > 1000 meters. $\Omega_{Arag}$ was at or below the sensitivity levels for both Atlantic cod and American lobster within their habitat depth ranges in western Gulf of Maine and off the coast of eastern Maine (Fig. \ref{fig:ne-oa}, right panels). These areas include Stellwagen Bank, slope waters south of Penobscot and Blue Hill Bays, and Wilkinson Basin and additionally, for Atlantic cod, slope waters south of Maquoit Bay and in waters of Jeffreys Ledge and Jordan Basin. The sensitivity levels of bottom $\Omega_{Arag}$ for Atlantic cod occurred in at least one of these areas during July 2007, August 2012, June 2013, June 2015, June and August 2016, June 2017, June and July 2018, August 2019, and July 2021, and for American lobster during June 2013, June 2016, June and August 2019, and July and August 2021.


```{r ne-oa, out.width = '80%', fig.cap = "Left panel: Bottom aragonite saturation state ($\\Omega_{Arag}$; summer only: June-August) on the U.S. Northeast Shelf based on quality-controlled vessel- and glider-based datasets from 2007-present. Right panel: Locations where summer bottom $\\Omega_{Arag}$ were at or below the laboratory-derived sensitivity level for Atlantic cod (top panel) and American lobster (bottom). Gray circles indicate locations where carbonate chemistry samples were collected, but bottom $\\Omega_{Arag}$ values were higher than sensitivity values determined for that species."}

#knitr::include_graphics("images/Saba_Fig_SOE_NEFMC - Grace Saba.png")

magick::image_read("https://github.com/NOAA-EDAB/ecodata/raw/master/docs/images/Saba_Fig_SOE_NEFMC.jpg")

```

### Ecosystem Productivity Indicators: phytoplankton, zooplankton, forage fish, fish condition

#### Phytoplankton

Phytoplankton support the food web as the primary food source for zooplankton and filter feeders such as shellfish. Numerous environmental and oceanographic factors interact to drive the abundance, composition, spatial distribution, and productivity of phytoplankton. In 2022, phytoplankton biomass (measured as chlorophyll a concentration) was above average in winter, but below average during the typical spring bloom period on GB.  Summer concentrations were variable but there was an anomalously high fall bloom throughout the region (Fig. \ref{fig:chl-weekly}).  Primary productivity (the rate of photosynthesis) was above average during the winter bloom and well above average from the late summer into winter in the Gulf of Maine (Fig. \ref{fig:pp-weekly}).

The seasonal cycle of size distribution of phytoplankton shows that the spring and fall bloom periods are dominated by larger-celled microplankton, while smaller-celled nanoplankton dominate during the warmer summer months. The proportion of the smallest phytoplankton, picoplankton (0.2-2 microns), is relatively constant throughout the year. In 2022, microplankton proportions in GB were above average during the winter, below average during the typical spring bloom period, and peaked again in late fall.  In the GOM, microplankton proportions were average or above average in all seasons, particularly in winter and fall (Fig. \ref{fig:weekly-phyto-size}).

```{r chl-weekly, fig.cap = "Weekly chlorophyll concentrations on Georges Bank (GB) and in the Gulf of Maine (GOM) are shown by the colored line for 2022. The long-term mean is shown in black and shading indicates +/- 1 sample SD.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-chl-weekly.R"), fig.width = 6, fig.asp=.36}
```

```{r pp-weekly, fig.cap = "Weekly primary productivity on Georges Bank (GB) and in the Gulf of Maine (GOM) are shown by the colored line for 2022. The long-term mean is shown in black and shading indicates +/- 1 sample SD.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-pp-weekly.R"), fig.width = 6, fig.asp=.36}
```

```{r weekly-phyto-size, fig.cap="The annual climatology (1998-2022) percent composition of the phytoplankton size classes on Georges Bank and Gulf of Maine based on satellite observations in the shaded portions. The 2022 proportions for the microplankton (>20 microns, green) and nanoplankton (2-20 microns, orange) are shown in the bold lines.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-weekly-phyto-size.R"), fig.width=6, fig.asp=.36}
```

#### Zooplankton
Zooplankton community diversity varies with changes in dominance of taxa (Fig. \ref{fig:zoo-diversity}). While still showing an overall increasing trend, the GB zooplankton community declined in diversity in 2021 due to the increase in abundance of the copepod *Centropages typicus* and salps. The GOM zooplankton community is usually dominated by *Calanus finmarchicus*, however their abundance decreased in 2021. This decrease plus an increase in abundance of other copepods (*C. typicus, Metridia lucens, Oithona spp.*), siphonophores, and pteropods resulted in high zooplankton diversity index in 2021.

```{r zoo-diversity, fig.cap="Zooplankton community diversity for Georges Bank (GB) and the Gulf of Maine (GOM).", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-zoo-diversity.R"), fig.width=6, fig.asp=0.4}

```

Decadal periodicity in the abundance of dominant copepods in the GOM and on GB has been previously reported, and these patterns continued to evolve into 2021. The abundance of *C. typicus* has been above average since 2012 in the GOM and on GB, and appears to be negatively correlated with *C. finmarchicus* abundance on GB (Fig. \ref{fig:zoo-abund}). *C. finmarchicus* has been below average in abundance since 2012 on GB following a period of high abundance between 2000-2010. *C. finmarchicus* also had high abundance in the GOM between 2000-2010, which corresponded to a period of recovery for right whales (Fig. \ref{fig:narw-abundance}). The abundance of *Pseudocalanus spp.*, an important prey item for cod larvae and other ichthyoplankton, has been below average on GB since 2000 and was below average in the GOM from 2000-2015, and most recently in 2021 the GOM larval fish diversity declined due to high abundance of hake (red, white, and silver) larvae.

```{r zoo-abund, fig.cap="Abundance Annomalies of three dominante zooplankton (\\textit{Calanus finmarchicus}, \\textit{Calanus typicus}, and \\textit{Pseudocalanus spp}.) on Georges Bank (GB) and the Gulf of Maine (GOM).", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-zoo-abundance-anom.R"), fig.width=6}

```

#### Forage Fish Energy Content
Nutritional value (energy content) of juvenile and adult forage fish as prey is related to environmental conditions, fish growth, and reproductive cycles. Forage energy density measurements from NEFSC trawl surveys 2017-2022 are building toward a time series to evaluate trends (Fig. \ref{fig:energy-density}). Data from the fall 2021 and spring 2022 survey  measurements were consistent with previous reports: the energy density of Atlantic herring increased to over 7 kJ/g wet weight, but was still well below that observed in the 1980s and 1990s (10.6-9.4 kJ/g wet weight). Silver hake, longfin squid (*Loligo* in figure) and shortfin squid (*Illex* in figure) remain lower than previous estimates [@steimle_energy_1985; @lawson_important_1998]. Energy density of alewife, butterfish, sand lance, and Atlantic mackerel varies seasonally, with seasonal estimates both higher and lower than estimates from previous decades.

```{r energy-density, fig.cap="Forage fish energy density mean and standard deviation by season and year, compared with 1980s (solid line; Steimle and Terranove 1985) and 1990s (dashed line; Lawson et al. 1998) values.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/macrofauna_MAB.Rmd-energy-density.R"), fig.width = 7.5, fig.asp = 0.6}
```

#### Forage Fish Biomass Index
The amount of forage fish available in the ecosystem combined with the energy content of the forage species determines the amount of energy potentially available to predators in the ecosystem. Changes in the forage base could pose a risk to managed and protected species production. A new spatially-explicit forage index estimated the combined biomass of 20 forage species using stomach contents information from 22 predatory fish species collected on bottom trawl surveys (Fig. \ref{fig:foragebio}). This new indicator shows an overall higher forage fish biomass in fall relative to spring. There is a long-term decreasing trend in the fall for GB and an increasing trend in the spring on GOM.  Changes in the distribution of forage biomass also affects predator distribution. Spatial subsets of this index were included in the bluefish research track stock assessment to investigate forage-driven changes in bluefish availability to recreational fisheries and surveys.  

```{r foragebio, fig.cap = "Forage fish index based on spring and fall survey predator diets.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/macrofauna_NE.Rmd-forage-index.R"), fig.width=6, fig.asp = 0.5}
```

#### Fish Condition
The health and well being of individual fish can be related to body shape condition indices (i.e., weight at a given length) such as relative condition index, which is the ratio of observed weight to predicted weight based on length [@le_cren_length-weight_1951]. Heavier and fatter fish at a given length have higher relative condition which is expected to improve growth, reproductive output, and survival. A pattern of generally good condition was observed across many species prior to 2000, followed by a period of generally poor condition from 2001-2010, with a mix of good and poor condition 2011-2019, and improved condition for many species in 2021 and 2022 (Fig. \ref{fig:gb-cf} & Fig. \ref{fig:gom-cf}). Preliminary results of synthetic analyses show that changes in temperature, zooplankton, fishing pressure, and population size influence the condition of different fish species. 

```{r gb-cf, fig.cap = "Condition factor for fish species on Georges Bank based on fall NEFSC bottom trawl survey data. No survey was conducted in 2020.", out.width = '100%'}

#knitr::include_graphics("images/GB_Condition_allsex_2022_viridis.jpg")

magick::image_read("https://github.com/NOAA-EDAB/ecodata/raw/master/docs/images/GB_Condition_allsex_2023_viridis.jpg")

```

```{r gom-cf, fig.cap = "Condition factor for fish species in the Gulf of Maine based on fall NEFSC bottom trawl survey data. No survey was conducted in 2020.", out.width = '100%'}

#knitr::include_graphics("images/GOM_Condition_allsex_2022_viridis.jpg")

magick::image_read("https://github.com/NOAA-EDAB/ecodata/raw/master/docs/images/GOM_Condition_allsex_2023_viridis.jpg")

```

#### Fish Productivity
We describe patterns of aggregate fish productivity on GB and the GOM with the small fish per large fish anomaly indicator, derived from NEFSC bottom trawl survey data (Fig. \ref{fig:productivity-anomaly-gb} & Fig. \ref{fig:productivity-anomaly-gom}). The indicator shows great variability with both regions being below average for much of the past decade.

```{r productivity-anomaly-gb, fig.cap = "Small fish per large fish biomass anomaly on Georges Bank. The summed anomaly across species is shown by the black line.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/macrofauna_NE.Rmd-productivity-anomaly-gb.R"), fig.width=5, fig.asp=.6}
```

```{r productivity-anomaly-gom, fig.cap = "Small fish per large fish biomass anomaly in the Gulf of Maine. The summed anomaly across species is shown by the black line.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/macrofauna_NE.Rmd-productivity-anomaly-gom.R"), fig.width=5, fig.asp=.6}
```

#### Common Tern productivity
2020 was a challenging year for terns raising chicks (Fig. \ref{fig:seabird-ne-productivity}).  While diet composition was similar to the long term average, the quantity of food readily available was apparently less than normal, particularly around the time of chick hatching.  This may have been confounded by cold, wet weather when chicks would normally be close to fledging in mid-to-late July. Anecdotal observations showed that feeding rates were low at both those times.

```{r seabird-ne-productivity, fig.cap = "Productivity of Common terns in the Gulf of Maine.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/macrofauna_NE.Rmd-seabird-ne-productivity.R"), fig.width=5, fig.asp=.4}
```

### Ecosystem Structure Indicators: distribution shifts, diversity, predators

As noted in the [Landings Implications section above](#landings), stocks are shifting their spatial distributions throughout the region. In aggregate, fish stocks are moving northeast along the shelf and into deeper waters.

Long-term trends show that zooplankton diversity is increasing on GB, while adult fish diversity is increasing in the GOM which also saw the highest zooplankton diversity index in 2022.  The rest of the diversity indices are stable over time with current values near the long term average (see [Diversity Indicators section, above](#diversity)).

Indicators for shark populations, combined with information on gray seals (see [Protected Species Implications section, above](#protected-species)), suggests predator populations in New England are either stable (sharks, Fig. \ref{fig:hms-cpue-sharks}) or increasing (gray seals, Fig. \ref{fig:seals}). Stable predator populations suggest stable predation pressure on managed species, but increasing predator populations may reflect increasing predation pressure.

```{r hms-cpue-sharks, fig.cap="Estimated number of sharks per unit effort from Highly Migratory Species Pelagic Observer Program data.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/macrofauna_MAB.Rmd-hms-cpue-sharks.R"), fig.width=6, fig.asp = .4}
```

Stock status is mixed for Atlantic Highly Migratory Species (HMS) stocks (including sharks, swordfish, billfish, and tunas) occurring in the New England region. While there are several HMS species considered to be overfished or that have unknown stock status, the population status for some managed Atlantic sharks and tunas is at or above the biomass target (Fig. \ref{fig:hms-stock-status} ), suggesting the potential for robust predator populations among these managed species. 

```{r hms-stock-status, fig.cap = "Summary of single species status for HMS stocks; key to species names at https://noaa-edab.github.io/tech-doc/atlantic-highly-migratory-species-stock-status.html.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/human_dimensions_MAB.Rmd-hms-stock-status.R"), fig.width = 6, fig.asp = 0.5}
```

As noted in the [Protected Species section](#protected-species), gray seal populations are increasing. Harbor and gray seals occupying New England waters are generalist predators that consume more than 30 different prey species. An evaluation of hard  parts found in seal stomachs showed that harbor and gray seals predominantly exploit abundant demersal fish species (i.e. red, white, and silver hake). Other relatively abundant prey species found in hard-part remains include sand lance, yellowtail flounder, four-spotted flounder, Gulfstream flounder, haddock, herring, redfish, and squids.

A stable isotope study utilizing gray seal scat samples obtained from Massachusetts habitats showed individual gray seals can specialize on particular prey [@hernandez_seasonal_2019]. It also found that gray seals vary their diet seasonally, focusing on demersal inshore species prior to the spring molt, and offshore species such as sand lance after molting. DNA studies on gray seal diet in GOM and Massachusetts state waters found spiny dogfish and Jonah crab present in gray seal scat samples [@ono_detecting_2019; @mccosker_metabarcoding_2020], with sandlance and menhaden dominant off Monomoy, MA [@flanders_utilizing_2020]. Skate and crab remains were also found in gray seal stomach remains. In contrast to direct feeding, it is uncertain if the presence of skates and crabs is due to secondary consumption or scavenging.

### Habitat Risk Indicators: habitat assessments, harmful algal blooms, fishing gear impacts

#### Habitat Assessments

The Northeast Regional Marine Fish Habitat Assessment (NRHA) is a collaborative effort to describe and characterize estuarine, coastal, and offshore fish habitat distribution, abundance, and quality in the Northeast. This includes mapping inshore and offshore habitat types used by focal fish species, summarizing impacts of habitat climate vulnerability on these species, modeling predicted future species distributions, and developing a publicly accessible decision support tool to visualize these results. This is a three-year project led by the New England and Mid-Atlantic Fishery Management Councils in collaboration with many partners including NOAA Fisheries^[https://www.mafmc.org/nrha].

#### New habitat model-based richness estimates

Species richness was derived from the NRHA habitat models for 55 common species sampled by the 2000-2019 spring and fall NEFSC bottom trawl surveys. The joint species distribution model controls for differences in capture efficiency across survey vessels, revealing patterns of declining richness in the Mid-Atlantic Bight and increasing richness in more northerly regions (i.e., the GOM; Fig. \ref{fig:habitat-richness}). These patterns reflect the decreasing probability of occurrence of cooler-water species in the south (Atlantic cod, American plaice, pollock, thorny skate) and the growing prevalence of warm-water species in the north (weakfish, spotted hake, and black sea bass), likely as a result of rising water temperatures.

```{r habitat-richness, fig.cap="Habitat model-based species richness for 55 common species sampled by NEFSC bottom trawl surveys.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_MAB.Rmd-habitat-richness.R"), fig.width=6, fig.asp=0.4}
```

#### Harmful Algal Blooms

Water quality as a component of habitat is of concern to managed species. Harmful Algal Blooms can degrade water quality. One example is *Alexandrium* blooms, which can result in Paralytic Shellfish Poisoning. *Alexandrium* cyst distribution and abundance are surveyed annually in the Gulf of Maine. After strong bloom events in 2005 and 2009, the time series suggests lower overall cyst abundance through 2021. However, bloom events and shellfishery closures do occur annually on a small scale and economic impacts can be substantial to inshore shellfisheries (mussels, clams, and quahogs). More information on Harmful Algal Blooms are available in the Synthetic Indicator Catalog^[https://noaa-edab.github.io/catalog/harmful-algal-blooms-alexandrium.html].

#### Fishing Gear Impacts

Estimates of the impacts of fishing gear on habitat are available through the habitat section of the Northeast Ocean Data Portal^[https://www.northeastoceandata.org/data-explorer/]. The data portal hosts selected outputs from the Northeast Fishing Effects Model which combines seafloor data (sediment type, energy regime) with fishing effort data to generate percent habitat disturbance estimates in space and time. More detailed information can be found in the Synthetic Indicator Catalog^[https://noaa-edab.github.io/catalog/northeast-fishing-effects-model.html].

### Implications

#### Links between climate change and managed species 

Estuarine, nearshore, and offshore habitats support many life stages of state and federally-managed species that are highly vulnerable to climate change. Overall, multiple drivers interact differently for each species producing a range of population impacts.

In addition to distribution shifts, climate change may shrink or fragment available habitat for species such as cusk [@hare_cusk_2012]. Projections of climate change scenarios appear to increase the vulnerability of cod to habitat loss on GB and particularly to the south, while warmer water temperatures in the GOM may decrease survival of early life stages of cod [@fogarty_cod_2007]. Both productivity and abundance decline for winter flounder with increasing water temperatures, potentially inhibiting the rebuilding of the stock despite reduced fishing pressure [@bell_rebuilding_2014].

#### Marine heatwave impacts
The adjustment to the marine heatwave methodology shows that extreme temperature events happen intermittently in many years, but have not been increasing over time in New England. While temperature variability in isolation has not changed, considering the overall increase in ocean temperature at both the surface and the bottom in the region, extreme events cause additional stress to organisms. While marine heatwaves lasting over days may disturb the marine environment, long lasting events such as the warming in 2012 (Fig. \ref{fig:heatwave}) can have significant impacts on the ecosystem [@gawarkiewicz_characteristics_2019]. The 2012 heatwave affected the GOM lobster fishery most notably, but other species also shifted their geographic distributions and seasonal cycles [@mills_fisheries_2013]. During the 2017 event, warm water fish typically found in the Gulf Stream were caught in shallow waters near Block Island, RI [@gawarkiewicz_characteristics_2019]. Ocean temperatures in 2022 rivaled or exceeded the record temperatures in 2012 in some seasons, but the impacts to fisheries have yet to be determined.

```{r heatwave, fig.width = 6, fig.asp = 0.35, fig.cap="Marine heatwave maximum intesity (left) and total days each year (right) in the Gulf of Maine.", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/LTL_NE.Rmd-heatwave-gom.R")}
```

#### Cold pool impacts
Changes in the cold pool habitat can affect species distribution, recruitment, and migration timing for many federally managed species. Southern New England-Mid Atlantic yellowtail flounder recruitment and settlement are related to the strength of the cold pool [@miller_state-space_2016]. The settlement of pre-recruits during the cold pool event represents a bottleneck in yellowtail life history, during which a local and temporary increase in bottom temperature negatively impacts the survival of the settlers. Including the effect of cold pool variations on yellowtail recruitment reduced retrospective patterns and improved the skill of short-term forecasts in a stock assessment model [@du_pontavice_incorporating_nodate; @miller_state-space_2016]. The cold pool also provides habitat for the ocean quahog [@powell_ocean_2020; @friedland_middle_2022]. Growth rates of ocean quahogs in the MAB (southern portion of their range) have increased over the last 200 years whereas little to no change has been documented in the northern portion of their range in southern New England, likely a response to a warming and shrinking cold pool [@pace_two-hundred_2018].

#### Distribution shift impacts

Trends for a suite of 48 commercially or ecologically important fish species along the entire Northeast Shelf continue to show movement towards the northeast and generally into deeper water (Fig. \ref{fig:species-dist}).  Habitat model-based species richness suggests shifts of both cooler and warmer water species to the northeast (Fig. \ref{fig:habitat-richness}). Similar patterns have been found for marine mammals, with multiple species shifting northeast between 2010 and 2017 in most seasons (Fig. \ref{fig:protectedspp-dist-shifts}, @chavez-rosales_detection_2022).

```{r protectedspp-dist-shifts, fig.cap="Direction and magnitude of core habitat shifts, represented by the length of the line of the seasonal weighted centroid for species with more than 70 km difference between 2010 and 2017 (tip of arrow).", code=readLines("https://github.com/raw/NOAA-EDAB/ecodata/master/chunk-scripts/macrofauna_MAB.Rmd-protectedspp-dist-shifts.R"), fig.width=7, fig.asp=0.8}
```

Shifting species distributions alter both species interactions and fishery interactions. In particular, shifting species distributions can alter expected management outcomes from spatial allocations and affect the efficacy of bycatch measures based on historical fish and protected species distributions.

#### Ecosystem productivity change impacts

Climate and associated changes in the physical environment affect ecosystem productivity, with warming waters increasing the rate of photosynthesis at the base of the food web. Warm temperatures can increase the rate of primary production; however they also increase stratification, which limits the flux of deep water nutrients to the surface. Thus most of the increases in summer production is often from smaller phytoplankton and may not translate into increased fish biomass. 

While krill and large gelatinous zooplankton have increased over time, smaller zooplankton periodically shift in abundance between the larger, more nutritious *Calanus finmarchicus* and smaller bodied copepods with no apparent overall trend. The nutritional content of forage fish changes seasonally in response to ecosystem conditions, with apparent declines in energy density for Atlantic herring and *Illex* squid relative to the 1980s, but similar energy density for other forage species. Overall forage fish biomass has fluctuated in both New England regions over time.  Some of these factors are now being linked to the relative condition of managed fishes.

The apparent decline in productivity across multiple managed species in New England, along with mixed fish conditions in 2022, also suggest changing ecosystem productivity at multiple levels. During the 1990s, high relative abundance of smaller bodied copepods and a lower relative abundance of *Calanus finmarchicus* was associated with regime shifts to higher fish recruitment [@perretti_regime_2017]. The unprecedented climate signals along with the trends toward lower productivity across multiple managed species indicate a need to continually evaluate whether management reference points remain appropriate, and to evaluate if ecosystem regime shifts have occurred or reorganization is in progress.